Abstract
The legume tree Schizolobium parahyba from the Brazilian Atlantic Forest shows young aerial organs covered with a sticky exudate. Aiming to clarify the functional aspects of the sticky secretions, we performed analyses on the dynamics of secretion through the plant development and characterized the chemical nature of the exudates by histochemical tests. We also studied the secretory tissue using light and electron microscopy. The production of the exudates starts soon after seed germination, being evident in the epicotyl but not in the hypocotyl and cotyledons. The secretory activity extends throughout the juvenile and pre-reproductive phase, in primary stems and leaf portions. After the first flowering, secretion was no longer observed. The lipid exudates are secreted by the epidermis and are composed of mixtures of essential oils and oleoresins. Modified plastids, extensive rough endoplasmic reticulum, proliferated smooth endoplasmic reticulum, enlarged vacuoles containing flocculant materials, membrane debris, and convoluted tubules/lamellae membranes covered with osmiophilic deposits are the main features of the secretory epidermal cells. Secretion exits the protoplast by exocytosis and accumulates in the cuticle, resulting in a sheath of concentric bands of electron-dense deposits, and is released by cuticle peeling. The hydrophobic nature of the secretion, which forms an impermeable layer on the epidermis of young organs, is a relevant attribute of the aerial organs of S. parahyba. In addition to protecting against desiccation, this exudate effectively captures particles and immobilizes insects and other arthropods.
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Introduction
Most of all the major families of vascular plants have species with some combination of sticky, slimy, or oily substances on their surfaces (LoPresti 2016). Sticky secretions on plants have different functions, such as capturing small animals (Adlassnig et al. 2010; Frenzke et al. 2016; Wilder 2019), indirect plant defense (LoPresti et al. 2015), spreading propagules, facilitating germination (Yang et al. 2010; De-Paula et al. 2015), collection of organic particles (Adlassnig et al. 2010), and collection of substrate or inorganic particles (LoPresti and Karban 2016). In most plant taxa with sticky exudates externally accumulated, secretion production and release occur most commonly in glandular trichomes (Fahn 1979; Voigt et al. 2020), causing plant surfaces to become sticky (Adlassnig et al. 2010; Falara and Pichersky 2012).
The adhesive properties of exudates are attributed to chemically diverse substances and include terpenoids, flavonoids, phenylpropanoids, alkaloids, fatty acid derivatives, and acylated sugars that confer mucilaginous or resinous properties to secretions (Werker 2000; Simoneit et al. 2008; Adlassnig et al. 2010; Betz 2010; Frenzke et al. 2016; Voigt et al. 2020). Despite the effectiveness of adhesive secretions in defending plants against herbivory (Levin 1976; Wagner 1991; Peiffer et al. 2009; Tian et al. 2012), specialized arthropods can move across sticky surfaces of plants without getting stuck (Voigt and Gorb 2008, 2010). Many species of invertebrates are known to colonize sticky plants to consume living and dead prey immobilized by adhesive secretions produced by glandular trichomes (Jiménez-Pomárico et al. 2019 and references therein). Biological adhesion has attracted much research interest in ecology, especially in plant–animal interactions (Wheeler and Krimmel 2015; Karban et al. 2019; Voigt et al. 2020). However, the morphological and cellular bases of the sticky exudates and their release to the plant surface are relatively understudied.
Plants collectively produce hundreds of thousands of low molecular but specialized metabolites, restricted to specific taxonomic groups and cell or tissue types (Fan et al. 2019). LoPresti et al. (2015) list about 120 genera distributed in 49 families of taxonomically unrelated angiosperms on which representatives of plants with sticky surfaces can be found, among them Leguminosae. Recent advances in next-generation sequencing and mass spectrometry technologies have unveiled the extraordinary metabolic diversity in all plants, such as acylsugars found in trichomes of Caryophyllaceae, Geraniaceae, Martyniaceae, Rosaceae, and Solanaceae (Liu et al. 2019). Acylsugars from the Solanaceae family—including plants of the Solanum, Physalis, Nicotiana, Petunia, and Salpiglossis genera, are produced in glandular trichome tip cells (Moghe et al. 2017; Fan et al. 2019).
Most of the studies on sticky exudates have been addressed to very specific stages in time and space, such as seed mucilage and leaf bud resins (in juveniles and spring budburst before reproduction), and little is known about the dynamic of secretion through the plant development, which is crucial for understanding their performance in heterogeneous habitats. Understanding the secretory process across the lifespan of the plant acquires particular importance in the ecological context to which the plant is subjected, especially during the seedling and juvenile phases. Seedlings and juvenile plants are usually subjected to environmental stresses, such as high irradiation, evapotranspiration and dehydration, and damage caused by trampling animals, herbivory, and pathogens (Oliveira 1999). All these agents are important potential causes of seedling mortality.
Schizolobium parahyba (Vell.) Blake, commonly known as ‘guapuruvu’ or ‘ficheira’, is a semi-deciduous legume tree reaching up to 20–30 m in height (Lorenzi 1992). Its natural distribution is irregular and discontinuous, widely found in forest gaps and edges in devastated ecosystems, as in the case of the Atlantic Forest of Brazil (Pinto and Brito 2003). Schizolobium parahyba is notable for its growth rate reaching 3 m per year, being of great importance in revegetation and landscaping projects (Lorenzi 1992; Freire et al. 2007).
In the course of a study on seedling and juvenile plants of Leguminosae woody species, Oliveira (1999) repeatedly found a sticky secretion covering the epicotyl and other young aerial portions of stem and leaves of S. parahyba. Motivated by these findings, we started discussing the origin of the superficial exudates and their potential roles during a particular and sensitive plant developmental stage.
In the present study, we performed analyses on the exudates and dynamics of secretion in loco in S. parahyba, investigated the chemical nature of the exudates, and identified the secretory tissues and their ultrastructural organization, aiming to clarify the morpho-functional aspects of the sticky secretions under a developmental point of view.
Materials and methods
Seeds of S. parahyba were collected in a remnant area of seasonal semi-deciduous forest located in Edgardia farm, in Botucatu municipality (22° 52ʹ S, 48° 26ʹ W, 786 m above sea level), in the central west region of São Paulo State, Brazil. The mean annual temperature is 20.3 °C, and the annual precipitation is 1428 mm. With a strong seasonality, rains occur in the summer (December–March) and drought in the winter (June–September), and with a small hydric deficiency from April to August (Cunha and Martins 2009).
The localization and sequential distribution of the secretory activity were described by observing in loco the seedlings and juvenile plants. For this, a lot of 50 seeds (five repetitions of ten units each) were placed in ger-boxes, between sheets of filter paper moistened with distilled water and kept in a germination chamber (BOD model NT708) at 25 °C ± 1, under continuous white fluorescent lighting (1000 lx, daylight). Subsequently, the seedlings were transplanted into black polyethylene bags with dimensions of 0.18 × 0.30 m and a capacity of 1.3 kg of the substrate, containing a mixture of soil (Red-Yellow Latosol with medium texture) and sand (1: 1 p/p), being kept in a greenhouse with shading nets (50% transmittance), and watered daily. Daily observations were made, considering two phases: seedling phase, from germination (determined by the protrusion of the primary root) to the expansion of the first photosynthetic leaf (eophyll), and the juvenile phase, from the seedling to the appearance of the first leaf with typical features of the species (metaphyll) (Oliveira 1999). At the same time, seedlings, juvenile, pre-reproductive (from the seedling to the first flowering) and adult (after the first flowering) specimens were observed at the field. Reference vouchers were deposited in the BOTU Herbarium, Department of Botany, Institute of Biosciences-São Paulo State University, UNESP.
The secretory tissues and cells in the seedlings, juvenile, and pre-reproductive plants were observed in samples from the epicotyl, other internodes of the primary stem, and leaves in the different developmental stages using stereoscopic microscopy (macroscopical analyses), scanning electron microscopy (SEM, surface examination), light microscopy (LM, anatomical and histochemical examination), and transmission electron microscopy (TEM, ultrastructural examination).
For anatomical analysis under LM, samples were fixed in formaldehyde, acetic acid, and 50% ethanol (FAA 50—Johansen 1940), dehydrated in a graded ethanol series, and embedded in methacrylate resin (Leica Microsystems Inc., Heidelberger, Germany). Cross and longitudinal sections (4–6 µm thick) were prepared with a rotary microtome (Leica RM2255) and stained with toluidine blue pH 4.7 (O’Brien et al. 1964). The sections were mounted on glass slides using a synthetic resin (Entellan New, Merck, Darmstadt, Germany). Observations and photographs were taken with a digital camera (Leica DC 300F) coupled with a light microscope (Leica DM5500B, Leica Microsystems, Wetzlar, Germany). Alternatively, hand-cut fresh sections were double-stained using astra blue and safranin (9:1 v/v; Bukatsch 1972); cell wall polysaccharides such as cellulose and pectins stain with astra blue, and safranin shows an affinity for lipids (Berlyn and Miksche 1976).
We registered the compounds present in the epidermal cells and in the superficial exudate using histochemical assays on sections of fresh materials obtained from the epicotyl and first internode above of juvenile plants (two months old). Sudan IV (Johansen 1940) detected total lipids and Nile blue (Cain 1947) for acidic (blue color) or neutral (pink color) lipids. Nadi’s reagent (a-naphthol and N, N-dimethyl-p-phenylenediamine) detected essential oils and oleoresin (David and Carde 1964). A 10% aqueous solution of ferric chloride highlighted phenolic compounds (Johansen 1940). A 0.02% aqueous solution of ruthenium red detected pectins (Jensen 1962). Lugol’s reagent highlighted starch grains (Johansen 1940). Standard control materials were prepared simultaneously. We examined and documented all specimens using a light microscope (Olympus BX41) equipped with a digital camera (Olympus C7070).
For the surface examination under SEM, samples were fixed in 2.5% glutaraldehyde in 0.1 mol L−1 phosphate buffer (pH 7.2), dehydrated in an ethanol series, and subjected to the critical drying point using liquid CO2. Samples were mounted on aluminum stubs, coated with gold (10 nm), and examined under a Quanta 200 scanning electron microscope (Fei Company, FEI, Gräfelfing, Germany) at 20 kV.
For ultrastructural characterization of the secretory cells under TEM, samples of epicotyl and first internode above were fixed in 2.5% glutaraldehyde in 0.1 mol L−1 phosphate buffer (pH 7.2) and left overnight at 4 °C. The material was then post-fixed in 1% osmium tetroxide (OsO4) solution in the same buffer for 2 h at room temperature, dehydrated in an acetone series, and embedded in epoxy resin (Araldite 502, Electron Microscopy Sciences, Hatfield, USA). Ultrathin sections were stained with uranyl acetate and lead citrate (Reynolds 1963). The sections were examined with a Tecnai Spirit TEM (FEI) at 80 kV.
Results
Location and temporal distribution of secretory activity
Schizolobium parahyba presented epigeal germination, and its cotyledons are leaf-like and photosynthetic (Fig. 1a). On the surface of the cotyledons and the hypocotyl, the secretory activity is absent. The surface of the epicotyl (Fig. 1a, b), subsequent internodes of the primary stem, pulvinus, and petiole (Fig. 1c) of the eophylls of S. parahyba seedlings was covered with a hyaline and sticky fluid, which can also be seen covering the epidermis of the young stem of juvenile and pre-reproductive plants (Figs. 1c, d, 2a–c). Soon after seed germination, the expanding epicotyl began to produce sticky secretion (Fig. 1a–c). The production of this secretion only occurred during organ expansion, both stem and leaves. Under SEM, the secretion was seen as a homogeneous material accumulation (asterisk) on the cuticle with a lattice aspect (Fig. 2d, e). In both the eophylls and metaphylls during pre-reproductive phase, secretory activity occurred in all the pulvinus and petiole, not having been observed in the leaflets blade. In the rachis just the abaxial surface presents secretory activity (Fig. 1d). The sticky exudate remained adhered to the surface of the immature portions of the organs, being gradually lost as they reached maturity, even in cases where the epidermis was persistent, as in the leaves. After the first flowering, sticky secretion was no longer observed. Therefore, in adult plants epidermis shows no secretory activity and a black indument (Fig. 1e) with simple non-glandular trichomes can be seen.
The presence of this secretion can trap particles, and immobilize small insects and mites, among other organisms which die attached to the plant (Fig. 2a–c) or manage to escape leaving parts of the body, such as wings and segments of the locomotor limbs (Fig. 2c). It was possible to observe visits by Brazilian stingless bees Tetragonista angustula Latreille (Apidae: Meliponina) in the field. These bees avoided the younger portions of the stem axis, in which the secretion is more abundant than the older, but they were observed collecting the secretion, especially in the rachis.
Structure, histochemistry, and secretion dynamics
In all sampled organs, secretory features of the epidermis can be recognized under the LM and TEM. Therefore, we chose to describe the epidermal tissue in the epicotyl samples and first internode above.
The epidermis is single-layered and constituted by juxtaposed, papilla-shaped columnar cells in a palisade-like arrangement (Figs. 3a–h, 4a). Scarce glandular trichomes consisting of a multicellular body with a cushion-like base were observed (Fig. 3a). The epidermal cells have dense content (Fig. 3a, b), thin walls, and a thickened cuticle (Fig. 3b). The cell content was stained purple with toluidine blue (Fig. 3a), pink with safranin (Fig. 3c), and reacted positively to the reagents to detect total and acid lipids (Fig. 3d, e), phenolic substances (Fig. 3g) and mucilage (Fig. 3h). The exudate deposited on the epicotyl surface reacted positively to the reagents to detect total and neutral lipids (Fig. 3d, e) and mixtures of essential oils and oleoresins (Fig. 3f). The results of histochemical tests carried out on the epidermis of the first internode above the epicotyl are summarized in Table 1.
Under TEM, epidermal cells of the epicotyl exhibited prominent nuclei, dense cytoplasm, and vacuoles of different sizes (Fig. 4a). The nucleus was spherical with heterochromatin lumps (Fig. 4a, b) and nucleolus (Fig. 4c). Numerous plasmodesmata (Fig. 4b) connect the epidermal and parenchyma cells. The plasma membrane had an irregular outline and, at some points, was detached from the cell wall forming small periplasmic spaces (Fig. 4b, c). Plastids with poorly developed inner membranes and filled with large translucent globules (Fig. 4b–d), extensive rough endoplasmic reticulum (RER) arranged in parallel rows along the anticlinal walls, mitochondria with prominent cristae (Fig. 4d), well-developed Golgi bodies with attached vesicles and polyribosomes (Fig. 4e) characterized the cytoplasm of the epidermal cells. Vesicles containing dense inclusion in close juxtaposition or fused with the plasma membrane were visible (Fig. 4f, g). At the same time, a network of cortical microtubules was seen longitudinally oriented along the anticlinal walls (Fig. 4f). Tubules and vesicles of smooth endoplasmic reticulum (SER) occurred in the cell periphery underlying the anticlinal walls, forming a network of reticular appearance (Fig. 4g). In these cells, plasmodesmata exhibited prominent pores filled with dark material.
At this time, in the peripheral cytoplasm facing the outer periclinal walls, there was an increase in the population of the Golgi bodies, SER tubules, and vesicles (Fig. 5a). Vacuoles containing membrane debris and osmiophilic deposits attached to the inner surface of the vacuolar membrane occurred in the peripheral cytoplasm (Fig. 5a). These vacuoles became enlarged and exhibited flocculant materials, membrane debris, and clusters of dense convoluted tubules/lamellae membranes covered with osmiophilic deposits (Fig. 5b). The convoluted membranes were attached to the inner surface of the vacuolar membrane (Fig. 5c) and seemed to have been originated from the intrusion and proliferation of the SER tubules into the vacuole.
Vacuoles containing flocculant inclusions were seen near the vacuole or in the peripheral cytoplasm near the outer epidermal cell wall (Fig. 5d). Flocculant materials and lipid accumulation, globose and translucent in appearance, occurred between the plasma membrane and the outer periclinal cell walls (Fig. 5d, e). Images suggesting the fusion of SER elements and vesicles with the plasma membrane were regularly observed (Fig. 5f). Deposits of dense materials occurred on the outer surface of the wall and scattered in the cuticle, often layered, resulting in a sheath of concentric bands in the cuticle (Fig. 5f) that had a frayed appearance (Fig. 5a, d, f).
During the secretion, we identified changes in the outer epidermal cell wall linked with the exudate release. The outer epidermal wall exhibited a complex structure and showed a clear gradation from a cellulose layer (facing the protoplast) followed by an intermediate zone and the cuticle proper at the outermost region. The intermediate zone presented osmiophilic material that protrudes through a cellulose microfibrils framework encrusted with large deposits of fatty substances to an outermost region (Fig. 5g). The outermost region of the cuticle (cuticle proper) is featured by a loose appearance and was free of the dense ramifications, exhibiting dense deposits with a granular appearance (Fig. 5h). During the secretory process, the cellulose layer exhibited a loose appearance and irregular thickness (Fig. 5i), and the cuticle showed signs of degradation (Fig. 5j). Lastly, the cuticle exhibited holes interspersed with remnants of the cuticular layer, while the outermost layer (cuticle proper) was no longer observed (Fig. 5k). As the secretion progressed, the cuticle appeared loose and porous (Fig. 5l), consistent with the lattice aspect seen in SEM (Fig. 2d, e).
Discussion
Structure–function relationships of the adhesive secretion in developing aerial organs
The occurrence of the epidermis specialized in the production of sticky fluid in the young aerial organs is of particular significance and constitutes a relevant attribute of plants of S. parahyba. The epidermal tissue entirely formed by secretory cells explains the long-term release of large amounts of this fluid in the developing aerial organs. Although many plants (20–30% of all vascular plants) have glandular trichomes, which often produce adhesive exudates (Duke 1994), this study demonstrated that glandular trichomes are very sparse in S. parahyba, and the ordinary epidermal cells were the main site of sticky fluid production. A continuous layer of sticky secretion covering an extensive area of the plant body, as we observed in S. parahyba, seems to be effective in catching and immobilizing arthropods. Although apparently less common, this strategy appears to be as efficient as catching insects by glandular trichomes as reported in different plant species (Voigt and Gorb 2010; Krimmel and Pearse 2013; LoPresti et al. 2015, 2018; Voigt et al. 2020). It is also important to consider that trichomes can be very sparse and have weak peduncles in some plant species, making prey capture less efficient.
The presence of adhesive fluid on the surface of the entire epicotyl in seedlings of S. parahyba can play a dual role in establishing new plants of this species. First, these superficial impermeable exudates constitute an effective barrier protecting the plumule and young stem against environmental stresses (e.g., Voigt et al. 2020), essential for seedling establishment when the most mortality occurs. The young phase is critical in the plant growth cycle since they depend greatly on the prevailing environmental conditions and determine the plant survival in natural habitats (Hadas 2005). Therefore, the occurrence of sticky exudates in the epicotyl surface could be significant to the immobilization of small insects and mites, among other organisms, which died attached to the epicotyl surface. The role of sticky secretions in indirect plant defense by providing predatory insects with entrapped insects has been reported for different plant species (Krimmel and Pearse 2013; LoPresti et al. 2015, 2018), contributing to reducing herbivory and increasing plant fitness. In general, the viscous secretion has no repellent properties but has immobilizing and toxicant effects on trapped animals (Sutherst et al. 1982).
The adhesive properties of the fluid covering the surface of the aerial organs of S. parahyba may be associated with the presence of lipids and terpenes (mixtures of essential oils and oleoresins) in this exudate, besides mucilage and phenolic substances detected in the epidermal cells. Natural adhesives consist of mixtures of different chemicals, frequently including terpenes (Betz 2010) and polyphenolics (Rischka et al. 2010). These compounds are bioactive and physiologically relevant in those plants bearing adhesive exudates (Jiménez-Pomárico et al. 2019).
Cytological events linked to the secretory process
The ultrastructural organization of the secretory epidermal cells in S. parahyba is similar to that described in previous reports for cytological events associated with the synthesis, transport, and release of mixed secretions composed by hydrophilic (mucilage) and lipidic substances (lipids and terpenes mixtures of essential oils and oleoresins) (Sadala-Castilho et al. 2016; Tresmondi et al. 2017). The abundance in ribosomal components is suggested to be connected with increased metabolic activity associated with the production of enzymes involved in the synthesis of secretion components and the cell wall modifications (Hall et al. 1981). Accumulation of Golgi bodies and vesicles in the vicinity of the cell walls is evidence of the role of this organelle in the synthesis and delivery of polysaccharides (Fahn 1979, 2000). The abundance of RER and SER elements in the peripheral cytoplasm and indications of Golgi body vesicles, or of SER tubules in juxtaposition to, or merging with, the plasma membrane, is compatible with subcellular localization studies, which show that the core reactions of the lipids and terpenes synthetic pathway occur at the endoplasmic reticulum (Nawrath et al. 2013). The juxtaposition of ER and plasma membrane observed here is evidence of the direct transfer of lipids from the ER to the plasma membrane. Modified plastids are involved in the fatty acid synthesis, giving rise to acyl chains that can be exported and modified by the key lipid synthesis enzymes located in the RER (Nawrath et al. 2013). Golgi and trans-Golgi network-mediated vesicle trafficking are involved in exporting secreted substances (polysaccharides and lipids) to the apoplast by exocytosis (McFarlane et al. 2014). In our study, the increase in the plasma membrane area originating periplasmic spaces indicates of merocrine secretion via exocytosis. The relationship between increased plasma membrane area and this pathway of cellular secretion has been highlighted in different types of glands and has important physiological significance in the secretory process (e.g., Fahn 1979, 2000; Evert 2006).
During secretion, the abundance of microtubules in the periphery of the cytoplasm is noticeable. The involvement of microtubules in organizing the organelle positioning, trafficking of cargos (particularly between the endoplasmic reticulum and the Golgi apparatus), the traffic through the Golgi apparatus itself, and the transport via exocytosis to the cell surface has been highlighted in the recent literature (Fourriere et al. 2020). In addition, the abundance of mitochondria with well-developed cristae can likely be associated with secretions transported through the plasma membrane and into the cell wall. This process involves ATP-binding cassette transporters and, possibly also, lipid transfer proteins (Nawrath et al. 2013).
We found that plasmodesmata connections were not interrupted by sticky secretions. In addition, plasmodesmata usually exhibited a large central cavity filled with dark content, consistent with active involvement in the symplastic pathway of the secretions. Studies using fluorescence redistribution after photobleaching (FRAP) have provided evidence that the ER membranes of plasmodesmata can serve as dynamic diffusion pathways for the movement of lipids and lipid signaling molecules between bordering cells (Epel 1994).
In S. parahyba, the secretion accumulates in the cuticular layer of the outer epidermal cell walls and is released by peeling the cuticle, as reported in colleters of Rubiaceae (Machado et al. 2012). This mechanism of secretion is distinct of those reported for glandular trichomes producing sticky secretion (Werker 2000; Jiménez-Pomárico et al. 2019), in which the exudate accumulates within a subcuticular space in the secretory head and then is released by cuticle rupture (Gregory et al. 1986; Pichersky and Gershenzon 2002; Peiffer et al. 2009) or through the cuticular pores (Wagner 1991; Wagner et al. 2004; Paiva 2016; Jiménez-Pomárico et al. 2019). Thus, we believe that the mechanism of elimination of the secretion by the epidermal cells could explain the abundance of exudate over the entire surface of developing organs in S. parahyba.
The relationship between secretory epidermis histochemistry, subcellular structures, and the mechanisms of sticky secretion is considered and helps us better understand the probable functions of the secretions. Despite the great diversity of secretory structures in Leguminosae, in vegetative and reproductive organs, including glandular trichomes, secretory epidermal cells, nectaries, idioblasts, canals, and cavities (e.g., Solereder 1908; Metcalfe and Chalk 1950; Uphof 1962; Lackey 1978; Leelavathi and Ramayya 1983; Marquiafável et al. 2009; Rodrigues et al. 2011; Matos and Paiva 2012; Marinho et al. 2015; Vargas et al. 2015, 2018), detailed studies regarding the lipid secretion processes and histochemistry of the secretory epidermis in legumes are scarce. Lipid secretions (neutral lipids and mixtures of essential oils and oleoresins) are common to other secretory structures in legume species (Vargas et al. 2018) and have been considered an important adaptive trait linked with defense function (Wink 2003). The specialized metabolites detected on the epicotyl and young stem surface of S. parahyba can function as a defense against microbial attacks and herbivores and help prevent damage by UV radiation (Harborne 1993). The external lipid secretion affects the survival capacity in environments with high light intensity and high temperatures (Tresmondi et al. 2017), as in the case of seedlings of S. parahyba. Due to their hydrophilic properties, the polysaccharides inside the epidermal cells can act to maintain the high water potential and protect the organs against desiccation damage (Sawidis 1998). This species is epigeous-phanerocotyledonar (Oliveira 1999) and is thus able to explore the multiple microhabitats of the environment (forest gaps and edges in devastated ecosystems), mainly those related to light conditions.
Conclusions and perspectives
As far as we know, sticky external secretions have been widely reported in various non-carnivorous plant genera and species (LoPresti et al. 2015, 2018), among which less than 10% appear to be shrubs or trees. Our results showing animal remnants accumulated on the sticky surface of seedlings and young plants from S. parahyba are consistent with the growing evidence that the stickiness provides an important and widespread indirect defense against herbivory (Karban et al. 2019). Therefore, the hypothesis that such plants benefit from the carrion of trapped insects makes much sense. Some sticky plants can absorb nutrients from the feces of predators, which are attracted by carrion trapped in sticky secretion (Anderson 2005), or as common in carnivorous plants, they can absorb nutrients directly from trapped insects (LoPresti et al. 2015). Regarding large tree species as S. parahyba, the relevance of this kind of nutrient acquirement seems unlikely, but this remains to be tested. For protocarnivorous plants inhabiting eutrophic or mesotrophic soils, Adlassnig et al. (2010) doubt if prey-derived nutrients were significant in meeting the nutritional demand of these plants, as opposed to carnivorous plants, in which significant amounts of nitrogen come from prey. To allow the absorption of nutrients from the carcasses of glued animals, the epidermis of the plant must be permeable; such permeability is characteristic in carnivorous plants (see Adlassnig et al. 2010 and references therein). In the case of S. parahyba, we did not observe any evidence of permeability, making the acquisition of nutrients unlikely. On the contrary, the hydrophobic nature of the secretion forms an impermeable layer that covers the epidermis. It is interesting to emphasize that seedlings and pre-reproductive plants are notably vulnerable phases and can survive in the undergrowth of a tropical forest for several years and wait for favorable light conditions to start growing (Halle et al. 1978; Whitmore 1990).
We want to emphasize that S. parahyba is a native pioneer tree of the Atlantic rainforest with a strong preference for clearings (Lorenzi 1992). According to Freire et al. (2007), the expansion of its populations may have occurred with deforestation since the eighteenth century. Thus, this species is classified as a seasonal semi-deciduous forest invader adapted to rapid colonization of forest gaps and edges or disturbed environments (Magalhães Filho 2013). In this context, the role of adhesive exudates on the young aerial organs has evident physiological and ecological implications. Although we did not develop a bioassay, our results suggest that secretion production on the entire surface of the developing organs from the seedling stage contributes to its pioneer and invasive character favoring local adaptability to numerous environmental impacts, mainly the light conditions and behavior of animal populations (Halle et al. 1978; Whitmore 1990).
Our study adds information to the understanding of the diversity of adhesive plant secretions, shedding light on particular structure–function relationships. In addition, they are essential for understanding the biological and ecological characteristics of forest species. Data presented here may provide useful information for future commercial development of biomimetic adhesives.
Data availability
Not applicable.
Code availability
The analysis code can be requested by emailing the corresponding author (silvia.machado@unesp.br).
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This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/ Edital Universal Proc. 401053/2016-4) and also by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES), Finance Code 001. EASP, DMTO, and SRM received research grants from CNPq (Proc. 305638/2018-1, 305686/2018-6, and 308982/2020-7, respectively).
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SRM, DMTO, and EASP conceived and designed the research. SRM, EASP and YC carried out the work. All the authors wrote the manuscript.
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Paiva, E.A.S., Oliveira, D.M.T., Canaveze, Y. et al. Adhesive secretion in Schizolobium parahyba (Vell.) Blake (Leguminosae: Caesalpinioideae): histochemical and morpho-functional characterization of this unusual feature in woody plants. Arthropod-Plant Interactions 16, 249–261 (2022). https://doi.org/10.1007/s11829-022-09888-y
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DOI: https://doi.org/10.1007/s11829-022-09888-y