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Morphology and Anatomy of Stem Mines in Cipocereus minensis (Wender.) Ritter (Cactaceae), an Endemic to Eastern Brazil

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Morphology and anatomy of stem mines in Cipocereus minensis (Wender.) Ritter (Cactaceae), an endemic species to Eastern Brazil Deusa D. Abreu1,2 Emilia Arruda3 G. Flávia A. Melo-de-Pinna1 J. Hugo Cota-Sánchez2,4 1 Universidade de São Paulo, Depto. de Botânica, CEP 05422-970, São Paulo, SP - Brazil

2 University of Saskatchewan, Department of Biology, Saskatoon, SK S7N 5E2 – Canada 3Universidade Federal de Pernambuco, Depto. de Botânica, CEP 50670-901, Recife, PE - Brazil

Abstract: mines are structures with the form of a cavity caused by consumption of host plant tissue by the insect’s miner larvae. Plant mines are more common in leaves, but in Cipocereus minensis, a species in which the leaves are modified spines, the miner activity is restricted to the stem. The aim of this paper was to document the morphological and anatomical differences in the infected and uninfected stems of C. minensis due to the feeding habit of the mining agent. Fresh tissue samples of non-mined and mined young stem of C. minensis were collected and examined in transverse sections. We hypothesize that the infection begins follow- ing mating when the females scratch the surface of the stem or while they feed on fruits and lay eggs, which subsequently develop into larvae, invading the stem. The insect’s miner larvae had mostly consumed the parenchyma tissue towards the center of the stem, and periderm formed along the entire path of the in- sect. This meristematic tissue or “wound periderm” is a common response for compartmentalization to isolate the damaged tissue, in this case the incubating chamber, in which the eggs will be placed. There were no signs of consumption of vascular tissue in the infested samples, further suggesting a compartmentalized infestation. The nest chamber was found in the stem pith region, with periderm surrounding an insect’s miner pupa in- side identified as a member of the Cerambycidae. The mining insect depends on a host plant to complete the life cycle; however, the nature of this partnership and the long-term effects of the insect on the plant tissue are unknown. The complex mechanisms by which herbivorous insects control the morphogenesis of the plant host are discussed. We propose that C. minensis has a recognition system to identify insect attack and evaluate the effectiveness of early response triggering compartmentalized defense mechanisms by protecting the injured area with a new layer of periderm.

Keywords: Stem anatomy, Cactaceae, Cerambycidae, Cipocereus minensis, controlled morphogenesis, recogni- tion system, stem mines.

Introduction defensive mechanisms. However, in spite of the ’ protective devices, insects are often successful Herbivory occurs in a wide group of insects in in fulfilling dietary and life cycle requirements. The predatory or parasitic forms. Among herbivorous in- relationship between mining insects and plants is ex- sects, mining species are remarkable because they are ceptional in terms of the insects’ specialization and adapted to specific environments and exhibit highly ability to survive in the microclimatic conditions, on specialized feeding habits. The complex nature of a selective and restricted diet provided by the host these plant-insect interactions involves intricate strat- plant (Csóka 2003; Schoonhoven et al. 2005). egies and adaptations that allow plants to overcome Plant mines are structures with the form of a cav- insect attack by deterring or reducing its effects using ity caused by consumption of host plant tissues by

4 Author for correspondence (Email: [email protected]) HASELTONIA VOL. 17. 2012 43 insect miner larvae living inside the plant. Insect the subfamily Opuntioideae, which has numerous mines are more common in leaves, but their occur- invasive species, in particular outside of their native rence has also been reported in root, stem, petiole, geographic range of distribution. In this regard, the flower, and fruit (Hering 1951; Weis and Berenbaum larvae of Cactoblastis cactorum Bergroth (Lepidop- 1989). The larva of the leaf miner is endophytic, lives tera) have been used for the biological control of inside the epidermal tissues, and depends on a host Opuntia monacantha (Willd.) Haw. in places where plant for shelter and food. The diet of the developing this species has colonized large areas (Lenzi et al. larva includes a selection of nutrients from the sur- 2006). However, the occurrence of cactus-feeding rounding subepidermal tissues of the host plant, in insects associated with members of the other cac- which the epidermis remains intact, and as it feeds, tus subfamilies, e.g., , Pereskioideae, and the larva forms small channels or even a small hollow Maihuenoideae, remains a mystery. Zimmerman and space, where it lives for part of its life cycle (Csóka Granata (2002) indicate that in the Cactaceae inter- 2003). nal cactus-feeding insects are more common than Mining insects have been documented in ap- external feeders, nearly 75% versus only 3%, respec- proximately 10,000 species and ca. 50 families en- tively. The remainder of insects associated with cacti compassing the orders Coleoptera (beetles), Dip- includes sapsuckers (15%) and fruit feeders (6%). In tera (flies), Hymenoptera (wasps), and Lepidoptera turn, mining insects represent a very small propor- (moths) (Connor and Taverner 1997; Csóka 2003). tion (only 1%) of the insect diversity associated with The species in these taxonomic orders undergo sev- cacti (reviewed in Zimmerman and Granata 2002). eral stages (instars) of metamorphosis during their The literature discussing the occurrence of mines life cycle. The largest order of insects, Coleoptera in tropical plants is restricted, and the anatomical (beetles), exhibits a great deal of ecological and mor- changes and effects on mined versus non-mined leaf/ phological diversity; however, few species have the stem are yet to be investigated. Much less is known mining habit. In fact, the most species-rich order about the anatomy and characteristics of the nest- of leaf-mining species is the Lepidoptera, but leaf- ing chambers of mining insects, in plants in general mining beetles have been reported in three families, and in cacti in particular. With the exception of a including jewel beetles (Buprestidae), leaf beetles few examples, the lack of factual information limits (Chrysomelidae), and weevils (Curculionidae) our understanding of the mechanism of action of (Csóka 2003). the mining agent and the degree of morphological Mines in plants have been documented early in transformation in the plant parts and tissues. Here the literature in several gymnosperm and angiosperm we present the case of a mining insect and convey families, such as the Rosaceae (Nawa 1916), Faga- information comparing the anatomy of mined and ceae (Suenaga 1938), Boraginaceae, Chenopodiaceae, non-mined tissues in the stem of Cipocereus minen- Dipsacaceae, Solanaceae (Hering 1951), Asteraceae sis (Wender.) Ritter, a columnar cactus endemic (Hering 1951; Melo-de-Pinna et al. 2002), Pinaceae, to eastern Brazil and easily identified by the bluish Betulaceae (Kumata 1964), Clusiaceae (Almeida- coloration of the fruits. Our goals were 1) to report Cortez and Melo-de-Pinna 2006), Malpighiaceae the occurrence of mines in the stem of C. minensis (Flinte et al. 2006), and the Apiaceae, Balsamina- caused by endophytic insect larvae, and 2) to high- ceae, Caryophyllaceae, Crassulaceae, Euphorbiaceae, light the morphological differences in the infected Fabaceae, Gentianaceae, Liliaceae, Poaceae, Rubia- and uninfected plants and to describe the nesting ceae, Salicaceae, Violaceae, among others (see Csóka area and the stem’s anatomical transformation due 2003). In spite of the vast number of mining insects to the feeding activity of the mining agent. A brief in plants, most studies have focused on the econom- discussion of the ecological and evolutionary advan- ic importance because several plant parts, e.g., leaves tages of this plant-insect association and the complex and fruits, of agricultural and ornamental species are mechanisms by which endophytic herbivorous insect damaged. On the other hand, mining insects have larvae control the morphogenesis of their host, is been used in the biological control of certain plants. also provided. In New Zealand, for example, Oemona hirta F. (Ce- rambycidae) causes the death of the stem of Car- Materials and Methods michaelia R. Br. (Fabaceae), a noxious plant (Syrett et al. 1999). The investigation of mines in plants Mined and non-mined stems of Cipocereus minen- is, therefore, significant not only to understand in- sis were observed in the municipality of Grão-Mogol sect biology and the implications of insect life cycle (16°35’S, 42°54’W) in the state of Minas Gerais, in biological control of fast-spreading weedy species, Brazil. The individuals of C. minensis (Fig.1A) were but also to unveil information regarding a putative found in areas with rocky substrate supporting Cer- coevolutionary relationship between the insect and rado (savanna) vegetation, an ancient biodiversity- the host plant and the plant responses and morpho- rich biome (Ratter et al.1997) that varies from pure genetic changes due to stimuli triggered by insect at- grassland to a plant community with medium-height tacks or injuries. trees with an almost closed canopy (Lopes and Cox In the Cactaceae studies dealing with insects 1977). The finding of anomalous, injured stems drew have been done in relation to pollination biology our interest, and we conducted surveys in different and biocontrol, the latter primarily investigated in populations in the nearby areas of distribution of 44 ABReu et al.—CIPOcereus stem anatomy

B C

A D E Figure 1. Cipocereus minensis (Cactaceae) showing stems affected by a larva and a pupa of Cerambycidae. (A) Habitat of plant growing under rocks. (B) Stem with external injury. (C) Longitudinal section with the pupal chamber. Note the tissue develop- ing inside of the chamber (arrow). (D) Transverse section of stem showing the pupa inside the chamber (arrow). (E) Detail of cerambycid pupa. Scale: 1 cm. this species in search of individuals with stem(s) ex- with a pupa) were observed in a population of ap- hibiting external wounding, which is an indication proximately 25 individuals. The pupa and larva of the presence of mines (Figs. 1B−D). found in the innermost part of the stem (pith) tissue Two fresh tissue samples of each, non-mined were unable to survive after being removed from the and mined stem, were collected and fixed in FAA nesting chamber and died before undergoing meta- (Formalin-Acetic acid-Alcohol) for 72 hours, then morphosis and completing the life cycle. As a result, dehydrated in ethanol series, followed by infiltration we were unable to fully identify this insect, which and embedding in histological paraffin according to belongs to the family Cerambycidae (Coleoptera). Johansen (1940). Transverse sections were cut with a Based on our population survey, the stem mine in rotary microtome, stained with astra blue and basic Cipocereus minensis is the result of the insect activity. fuchsin, and mounted in synthetic resin (Kraus et Evident damage (a black dot) was observed in the ex- al. 1998). Sectioned material was analyzed with a ternal part of the mined stem where the female in- digital camera system IM50 and the Leica DMLB sect possibly laid the eggs (Fig. 1B). Larvae develop- microscope. Voucher specimens (D. D. Abreu, 02) ing from the eggs feed on plant tissue and eventually of mined and non-mined stems were collected and reach the stem’s pith region. A larva also devours part deposited in the herbarium of the University of São of the pith parenchyma tissue, building a chamber in Paulo (SPF). A larva and a pupa of the mining insect which the pupa nests (Figs. 1C−E) and spends the were found during voucher preparation in the core greater part of its life cycle. The chamber is approxi- region of the stem. Both larva and pupa (Fig. 1E) mately 10 cm long and 2 cm wide. were collected for identification. Anatomy of the non-mined stem: Analyses of trans- verse sections of non-mined stems indicate general Results characteristics present in the Cactaceae. The epider- mis is uniseriate, but the cortical region has an ex- Population sampling and identification of the ternal multiseriate hypodermis (Fig. 2A; Table 1) mining insect: The proportion of affected plants with cells of irregular thickness in the primary walls detected during the field survey was low. Only two (Figs. 2A, 2B), also characterized by the presence of mined individuals (one with a larva and another prismatic druses. The rest of the cortex is organized HASELTONIA VOL. 17. 2012 45

A

B Figure 2: Transverse sections of non-mined stem of Cipocereus minensis. (A) Uniseriate epidermis and cortex with outermost multiseriate hypodermis and mucilage cells. Note the druses in the cortex (arrows). Scale: 400 µm. (B) Detail of the vascular system and pericyclic fibers (arrow) in non-mined stem. Scale: 1000 µm. Hy: hypodermis. Mc: mucilage cells. 46 ABReu et al.—CIPOcereus stem anatomy

Characters Non-mined stem Mined-stem Epidermis Uniseriate Uniseriate (except next to coleopteran entry area) Periderm Absent Present next to coleopteran entry area Hypodermis Multiseriate Affected only next to coleopteran entry area Parenchyma tissue (cortical and pith Normal Affected along the entire path of the mining insect regions) Druses Present Present Vascular Tissue Present Not affected Nesting Chamber Absent Present with surrounding periderm

Table 1: A comparison of the anatomical features between non-mined and mined stem of Cipocereus minensis. into two regions: the palisade cortex located in the suggested that the presence of druses embedded in outermost part and the water-storage parenchyma in the cells deter phytophagous insects and protect the the inner portion. In the cortex and in the pith, mu- plant against excessive incidence of sunlight (Gibson cilage cells and collateral cortical bundles were pres- and Nobel 1986; Mauseth and Ross 1988; Mauseth ent. In the vascular system pericyclic fibers (arrow in 1989; Soffiatti and Angyalossy 2003; Yoshikawa et Fig. 2B) were present outside the primary phloem, al. 2005). In spite of the protection and mechanical which appears collapsed. The young stem was in the barrier against extrinsic biotic and abiotic agents pro- secondary growth, with non-fibrous wood consisting vided by the plants’ epidermis, hypodermis and other of vessel elements and matrix of parenchyma cells. structures, our study suggests that the artillery of the The phloem consisted of sieve tube elements and pa- mining agent is, nevertheless, strong enough to break renchyma cells. The ray cells remain unlignified in through some areas of the stem of C. minensis. In young stem (Fig. 2B). fact, the formation of periderm, the plant’s response to wounding, in the region through which the cole- Anatomy of the mined stem: The young mined opteron enters is evident in the affected stem areas. stem displays some differences in relation to non- This is unusual because the presence of periderm has mined stem, in the dermal tissue, in particular, next only been reported in the basal region of the stem of to the coleopteron entry area, and portions of the C. minensis (Soffiatti and Angyalossy 2003) but not cortical and pith tissues, which the insect consumed in the middle or upper portions of young stem as (Figs. 3A−F). In this case, periderm forms along the found in this study. This finding suggests that both entire active path of the mining insect (Table 1) in young and mature stem portion are capable of devel- response to the wounding. Observations of the trans- oping a layer of periderm. verse sections of the mined stem indicate that once For newly hatched plant-feeding insects, the diet inside the plant tissue, the larvae consume some selection (host plant) is primarily a critical parental cortical and pith parenchyma tissues (Figs. 3A, 3B) choice at the moment of oviposition (Schoonhoven while moving inside in the direction of the pith re- et al. 2005). Soon after oviposition, the stem under- gion. However, only in the pith region, some cells goes modifications due to the incursion of the Cer- convert to phellogen, a cell layer responsible for the ambycidae. In general, the cactus stem is organized development of periderm surrounding the chamber into palisade cortex and water-storage cortex with where the larva undergoes metamorphosis (Figs. 1C, cortical vascular bundles. However, in the mined 1D; Figs. 3E, 3F). During this feeding period the stem, the infection of the Cerambycidae is compart- vascular system remains unaffected. In fact, at this mentalized: the insect feeds only on parenchyma tis- stage, the vascular system shows evidence of second- sue as it moves towards the stem’s pith region, where ary growth as noted by the axial xylem consisting the larva eventually forms the mine and the vascular primarily of vessel elements and fibers (Figs. 3E, 3F). tissue is not consumed, hence remaining unaffected. Further, there is development of periderm in the Discussion stem of C. minensis with concomitant formation of the insect mine made of sclereids. This meristematic Several putative defense mechanisms against tissue or “wound periderm” is a common response predators and diseases have been identified in cacti. with the effect of compartmentalization to isolate Spines and the thick cuticle are the primary barri- the damaged tissue (Shigo, 1984), in this case the ers, but chemical defenses within the cortex, such incubating chamber, where the eggs will be placed. as alkaloids and mucilage, are often toxic to insects This tissue likely formed after the insect entered into (Gibson and Nobel 1986). In addition, it has been the pupal instar, the metamorphic period in which HASELTONIA VOL. 17. 2012 47

Figure 3: Transverse sections of mined stem of Cipocereus minensis. (A) Mined stem beginning the formation of the wound phellogen induced by the presence of the stem miner. Note the periderm. Scale: 200 µm. (B) Dermal tissue system of the region affected by the coleopteran. (C) Detail of the cortical region affected by the coleopteran (arrow). Scale: 1000 µm. (D) Development of the mine caused by the cerambycid larva (arrow). (E−F) Mined stem with vascular system not affected by the coleopteran, and chamber in the medullary region of the stem. Scale: 400 µm. Hy: hypodermis. Ch: chamber. Cp: cortical parenchyma. Mc: mucilage cells; Pe: periderm. Vs: vascular system. the insect does not eat and the plant develops scler- tiated secondary growth, but the prevalence of soft eids in the walls of the nest chamber. Similar find- tissue may have facilitated the migration of the min- ings have been described in Richterago riparia Roque ing agent from the cortical to the pith region of the (Asteraceae) (Melo-de-Pinna et al. 2002) and Vismia stem. Also, the feeding habit of the mining insect guianensis (Aubl.) Seem (Clusiaceae) (Almeida-Cor- suggests a preference for soft tissue because through- tez and Melo-de-Pinna 2006). Our findings indicate out the whole path of feeding and migration through that the vascular system of the mined stem had ini- the plant tissues there was no consumption of lig- 48 ABReu et al.—CIPOcereus stem anatomy nified cells from the vascular system. This apparent ber species. However, some mining insects have been predilection for soft plant tissues is in disagreement used in biological control of weedy/exotic plants, for with Martins’s (1997) classification of this insect as a instance, control of Cytisus Desf. in the US, New wood consumer, a characteristic feeding habit of nu- Zealand and Australia (Syrett et al.1999), the use of merous Cerambycidae. Hexomyza sarothamni (Diptera) to control Acacia lon- The origin of this plant-insect relationship is un- gifolia (Andrews) Willd. in South Africa, and biocon- known, but it might depend to a great extent on the trol of invasive cacti with the larvae of Cactoblastis maternal selection of host plant for oviposition. We cactorum (prickly pear moth), a lepidopteran preda- believe that the biology of this insect is similar to an- tor − not a mining agent − of Opuntia monacantha in other member of the Cerambicydae, viz., Trachyderes Brazil (Lenzi et al. 2006). Based on our observations, mandibular, which is found in the columnar saguaro we include the C. minensis-insect relationship in cactus Carnegiea gigantea (Engelm.) Britton & Rose. the destructive category because regions of the stem According to Goldsmith and Alcock (1993), the T. show serious injury. These observations, coupled mandibular males and females feed on the pulp of C. with the anatomical damage observed, indicate that gigantea fruits. During the feeding period, male com- in the long-term, the loss of large portions of the petition is intense in protecting the targeted fruit. stem could result from the mining insect’s activity. The fruits serve to attract the females for mating pur- Disease agents affecting and/or controlling plant poses because feeding females are sexually receptive morphogenesis are poorly known; however, several and rarely evade males. Another strategy to invade physiological networks and signal-activated mecha- host plants has been documented in the Cerambyci- nisms work in synchrony to express different abnor- dae, involving the flower as the target area to lay eggs, mal forms that shelter (host) alien organisms. For thus facilitating the entrance of the larva into the instance, gall morphogenesis involves a cascade of host stem via soft plant tissues (Kirk and Wapshere events, including stimulus recognition, signal trans- 1979). Other Cerambycidae have been observed in duction and gall growth in host plants (Raman, association with flowers and fruits of columnar cacti 2011). In the Cactaceae, one of the most interesting (Rocha et al. 2007). We hypothesize that a similar cases of plant parasitism is that of the endophytic premise applies to C. minensis and that the process mistletoe Tristerix aphyllus (Miers ex DC.) Barlow & of invasion of host tissue begins following mating, Weins, which parasitizes the columnar cactus Tricho- when the females scratch the surface of the stem (or chiloensis (Colla) Britton & Rose (= Echinopsis while they feed on fruits) and lay eggs, which sub- chiloensis (Colla) Friedrich & G.D. Rowley) (Maus- sequently develop into larvae, the prime instar stage eth 1990; pers. comm.). The attack of microbial invading the cactus stem. pathogens and herbivorous insects can have delete- Although the exact origin of the mining habit in rious effects on the host plant’s growth and impair insects is a matter of discussion, it has been hypoth- reproduction. Plants have evolved to express several esized that it evolved at the beginning of the Creta- protective mechanisms induced by the alien organ- ceous (Labandeira et al. 1994), but Csóka (2003) ar- ism to counteract the effect of pathogenic or herbivo- gues that according to the fossil record, lepidopteran rous injury. Although the molecular mechanisms of mines first appeared in the Jurassic. According to action involved in activating plant defense responses Connor and Taverner (1997), endophytic insect are not entirely understood, it has been shown that miners represent an adaptive innovation compared these depend on the natural immunity of individual with other larvae of insects that consume only the cells and on systemic signals, such as insect saliva on external part of the plant tissue. Furthermore, the the wounded tissue or emanating from infected sites mining habit may have protective benefits for the (Jones and Dangl, 2006; Raman, 2011). According host plant against attack by natural enemies, e.g., to Glazebrook (2005), once virulence activators (ef- predators, pathogens, and parasites, while the insect fector molecules) are recognized by the plant’s im- benefits from the intrinsic quality of habitat and mune system, resistance or R genes are activated to reduction in the impact of physical environmental limit pathogen growth. R genes are associated with parameters (e.g., hygrothermal balance, ultraviolet the production of reactive oxygen species and the ac- radiation, wind and rain) which adversely affect in- tivation of salicylic acid, both of which are required star development (Goldsmith and Alcock 1993). It is in a programmed hypersensitive cell death or hyper- doubtful that this cerambycid miner is advantageous sensitive response (HR) process and the expression for C. minensis, but it is possible that it aids in seed of pathogenesis-related proteins contributing to re- dispersal because female Cerambycidae move from sistance to prevent the foreign agent from accessing one cactus to another in search of new fruits for food water and nutrients. The cascade of these defense (Rocha et al. 2007). responses is vital for the plant’s fitness and evolution- Within the Cerambycidae some mining species ary fate (Katagiri and Tsuda, 2010). have significant adverse effects in agriculture; e.g., A large proportion of the studies involving mo- Hedypathes betulinus damages leaves of Ilex paraguar- lecular recognition and the signaling network have iensis A.St.-Hil, leading to lower yields of yerba mate been done in Arabidopsis. Nevertheless, we speculate and associated financial losses (d’Avila et al. 2006). that C. minensis has a recognition system to iden- About 20% of the European longhorn beetles are tify insect attack and to evaluate the effectiveness of undesirable in forestry because they are pests of tim- early response, triggering compartmentalization de- HASELTONIA VOL. 17. 2012 49 fense mechanisms that protect the injured area with zilian Atlantic forest. Brazilian Journal of Biology 66: a new layer of periderm. For instance, the chamber 759−763. formed as a result of the insect’s damage is character- Connor EF, Taverner MP. 1997. The evolution and ized by a relatively thick layer of periderm (Figs. 3E, adaptive significance of the leaf-mining habit. Oikos 3F), quite likely as the plant’s resistance response to 79: 6−25. prevent the spread of the injury, in particular to the Csóka G. 2003. Levélaknák és levélaknázók − Leaf mines vascular bundles and other soft tissue. The cell death and leaf miners. Hungarian Forest Research Institute. in C. minensis is equivalent to the HR reported in Erdészeti Turományos Intézet, Agroinform Kiadó, Bu- Arabidospsis by Glazebrook (2005). On the other dapest. hand, the haustorium of the parasitic mistletoe Tris- d’Avila M, Costa CE, Guedes JVC. 2006. Bioecologia terix aphyllus spreads through the vascular bundles of e manejo da broca-da-erva-mate, Hedypathes betulinus the host, the cactus Trichocereus chiloensis (Mauseth, (KLUG, 1825) (Coleoptera: Cerambycidae). Ciência 1990). In this infection there is no obvious reaction Florestal 16: 233−241. on the part of the cactus, and just ordinary cortex or Flinte V, Araujo CO, Macedo, MV Monteiro RF. pith parenchyma forms right up to the Tristerix pa- 2006. Insetos fitófagos associados ao murici da praia, renchyma. Unlike C. minensis, T. chiloensis is unable Byrsonima sericea (Malpighiaceae), na restinga de Ju- to recognize the “attack” as no periderm is formed. rubatiba (RJ). Revista Brasileira de Entomología 50: However, if the mistletoe dies off, then the cactus 512−523. wound forms cork around the parasite tunnel. In the Gibson A, Nobel P. 1986. The cactus primer. Harvard older literature, these have been described as reac- University Press, Cambridge. tions to insects, but it might be the result of mistle- Glazebrook J. 2005. Contrasting mechanisms of defense toe infection (J. Mauseth, pers. comm.). against biotrophic and necrotrophic pathogens. An- In conclusion, the insect miner larva feeds only nual Review of Phytopathology 43:205–227. on parenchyma tissue toward the center of the stem. Goldsmith SK, Alcock J. 1993. The mating changes The periderm along the entire path of the mining of small males of the Cerambycid beetle Trachyderes insect and surrounding the nesting chamber repre- mandibularis differ in different environments (Cole- sents a response of the cactus to action of the insect. optera: Cerambycidae). Journal of Insect Behavior 6: This effective plant response leads to the isolation of 351−360. different plant tissues in different compartments to Hering EM. 1951. Biology of the leaf miners. 1st Ed. prevent further damage. While the mining insect Springer, Berlin. depends on its host plant to complete the life cycle, Johansen DA. 1940. Plant microtechniques. McGraw- the nature of this partnership and the long-term ef- Hill, New York. fect of the insect on the plant tissue are obscure. The Jones JD, Dangl J.. 2006. The plant immune system. investigation of several insect and plant attributes, Nature 444: 323−329. such as physiology and stimuli recognition, behavior, Katagiri F, Tsuda K. 2010. Understanding the plant im- breadth of diet, life cycle, plant anatomy and chemi- mune system. Molecular Plant-Microbe Interaction 23: cal composition, is critical to establishing the foun- 1531–1536. dations of the biology and evolution of this seem- Kirk AA, Wapshere AJ. 1979. The life history and host ingly complex plant-insect interaction system and to specificity the Echium Borer, Phytoecia coerulenscens understanding the different strategies plants use to (Col.: Cerambycidae). Entomophaga 24: 423−430. alleviate and neutralize stress originating from alien Kraus, JE, Sousa HC, Rezende MH, Castro NM, organisms. Vecchi C, Luque R. 1998. Astra blue and basic fuc- sin double staining of plant materials. Biotechniques Acknowledgements and Histochemistry 73: 235. Kumata T. 1964. Description of a new stem-miner of co- We are grateful to A. Davis, D. Litwiller, M. niferous tree from Japan (Lepidoptera: Gracillariidae). Pace, M. Silva, and M. Souza for suggestions on Insecta Matsumurana 27: 31−34. early drafts of the manuscript. To J. Mauseth and Labandeira CC, Dilcher DL, Davis DR, Wagner DL. one anonymous reviewer for valuable feedback. S. 1994. Ninety-seven million years of angiosperm-insect A. Vanin and U. C. Martins assisted in the identifi- association Paleobiological insights into the meaning cation of the Cerambycidae, and D. Zappi assisted of coevolution. Proceedings of the National Academy of with the identity of the plant. The Fundação de Am- Sciences (USA) 91: 12278−12282. paro a Pesquisa do Estado de São Paulo (Grant No. Lenzi M, Soares J, Orth AL. 2006. Predação de Opun- 04/05344-0) and the Conselho Nacional de Desen- tia monacantha (Willd.) Haw. (Cactaceae) por Cacto- volvimento Científico e Tecnológico provided finan- blastis cactorum (Lepidóptera: Pyralidae) em restingas cial support for this research. da Ilha de Santa Catarina, sul do Brasil. Biotemas 19: 35−44. Literature Cited Lopes AS, Cox FR. 1977. Cerrado vegetation in Brazil: an edaphic gradient. Agronomic Journal 69: 828−831. Almeida-Cortez JS, Melo-de-Pinna GFA. 2006. Mor- Martins UR. 1997. Cerambycidae sul-americanos (Coleop- phology and anatomy of a leaf mine in Vismia guia- tera). Sociedade Brasileira de Entomologia, São Paulo. nensis (Aubl.) Choisy (Clusiaceae) in fragment of Bra- 50 ABReu et al.—CIPOcereus stem anatomy

Mauseth JD. 1989. Comparative structure-function studies within a strongly dimorphic plant, Melocactus inortus (Cactaceae). Bradleya 7: 1−12. Mauseth JD. 1990. Morphogenesis in a highly reduced plant: the endophyte of Tristerix aphyllus (Lorantha- ceae). Botanical Gazette 151:348–353 Mauseth JD, Ross RG. 1988. Systematic anatomy of the primitive cereoid cactus Leptocereus quadricostatus. Bradleya 6: 49−64. Melo-de-Pinna GFA, Kraus JE, Menezes NL. 2002. Morphology and anatomy of leaf mine in Richterago riparia Roque (Asteraceae) in the campos rupestres of Serra do Cipó, Brazil. Brazilian Journal of Biology 62: 179−185. Nawa U. 1916. On the pests of apple in Hida district of Japan. Insect World 20: 274−281. Raman, A. 2011. Morphogenesis of insect-induced plant galls: facts and questions. Flora 206: 517−533. Ratter JA, Ribeiro JF, Bridgewater S. 1997. The Bra- zilian Cerrado vegetation and threats to its biodiver- sity. Annals of Botany 80: 223−230. Rocha EA, Machado IC, Zappi DC. 2007. Floral bi- ology of tuberculatus (Werderm). Byles & Rowley: a bat pollinated cactus endemic from the “Caatinga”in the northeastern Brazil. Bradleya 25: 129−144. Schoonhoven LM, van Loo JJA, Dicke M. 2005. In- sect-plant biology. 2nd. Ed. Oxford University Press, Oxford. Shigo, AL.1984. Compartmentalization: a conceptual framework for understanding how trees grow and de- fend themselves. Annual Review of Phytopathology 22: 189−214. Soffiatti P, Angyalossy V. 2003. Stem anatomy of Cipocereus (Cactaceae). Bradleya 21: 39−48. Suenaga H. 1938. On the chestnut-bark miner. Acro- cercops sp. Japanese Journal of Applied Zoology 10: 108−109. Syrett P, Fowler SV, Coombs EM, Hosking JR, Mar- kin GP, Paynter QE, Sheppard W. 1999. The po- tential for biological control of Scotch broom (Cytisus scoparius) (Fabaceae) and related weedy species. Bio- control News and Information 20: 17−34. Weis AE, Berenbaum MR. 1989. Herbivorous insects and green plants. In: Abrahamson WG (ed) Plant- animal interactions. McGraw Hill Book Co, New York. Yoshikawa RCS, Soffiatti P, Angyalossy V. 2005. Stem and root anatomy of Melocactus bahiensis and Melocactus concinnus (Cactaceae, Subfamília Cactoi- deae, Tribe ). Revista de Biologia Neotropical 27: 45−52. Zimmerman HG, Granata G. 2002. Insect pests and diseases. In: Nobel, PS (Ed), Cacti: biology and uses. University of California Press, Los Angeles.

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