Biomimetically Structured Lamellae Assembly in ... - ACS Publications

May 11, 2018 - ... of several polymers including polyethylene.12−22 One view proposes that lamellar .... assembly of ring-banded polymer spherulites...
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Biomimetically Structured Lamellae Assembly in Periodic Banding of Poly(ethylene adipate) Crystals E. M. Woo,* Kai-Cheng Yen, Yu-Ting Yeh, and Lai-Yen Wang Department of Chemical Engineering, National Cheng Kung University, Tainan 701-01, Taiwan ABSTRACT: Nature tends to assemble hierarchical structures in similar ways to achieve compactness and functions. This work probes the interior lamellae assembly of crystalline spherulites of poly(ethylene adipate) (PEA) with striking birefringence patterns versus some known biological structures for optical color diffraction. Threedimensional dissecting onto interior lamellar structures of spherulites in poly(ethylene adipate) (PEA) in bulk forms crystallized at 28 ± 3 °C were studied in correlation with thin-film forms. Interior morphology in bulk PEA samples revealed periodic hemisphere or arc-shaped layers resembling corrugate boards with liner-flute medium alteration. Interior spherulites clearly expose that the lamellae within the intralayer are kebabs (plates) in the radial direction while the interlayer region are thin sheaths (fibrils) composed of cilia-like lamellae in the tangential direction. The interior repetitive lamellar assembly of PEA banded spherulites in displaying periodic optical birefringence patterns is proven to highly resemble those in many biological structures for iridescence light interference.

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INTRODUCTION Bioresourceful or petro-based aliphatic polyesters and their copolyesters, owing to potential biodegradability and biorelated applications, have been widely studied for synthesis, crystallization, phase behavior, or supramolecular structures.1−11 Rarely, if any, have the crystals of these polyesters been investigated to show periodic assembly patterns with nano- to micrometer structures that can be biomimetically comparable to some biological species in performing specific functions related to optical patterning. For a long time of unsettlement, interpretations on the formation of ring-banded morphology in polymer spherulites have been debated for decades. Lamellar helical-twisting among all the proposed mechanisms had been one of the most adapted models to account for the formation of the concentric ring bands in spherulites of several polymers including polyethylene.12−22 One view proposes that lamellar twisting is associated with features that exist during growth or are generated by the growth process itself;20 others describe that twisting is associated with the morphology or structures of lamellae themselves that may be associated with screw dislocations21 or surface stresses at the fold surface.22 Nevertheless, more recent studies have pointed out that alternative views might be better for explaining the periodic optical patterns in polymer spherulites. Biocopolyesters have been the recent focus of investigations on ring-banded morphological features. Xu et al.23,24 have characterized banded spherulites of poly(3-hydroxybutyrate-co-hydroxyhexanoate) [P(HB-co-HHx)] using in situ atomic force microscopy (AFM) and found that the lamellae in the banded spherulites of P(HB-co-HHx) exhibit complicated growth behaviors: twisting, bending, backward growth, and branching, etc. In addition, the lamellae of P(HB-co-HHx) spherulites continuously twist to show alternating edge-on and flat-on orientations © XXXX American Chemical Society

along the radial direction. Continuous helical twisting has been a popularly proposed mechanism since 1960. Banded morphology in poly(trimethylene terephthalate) (PTT) display vividly colorful banding in POM, which is attributed to lamellar twisting by several investigators. Ho et al.,25 as one of proponents for the continuous helical twisting model of Keith−Padden,12−15 have explained that the lamellar twisting in PTT may be caused by the tilted chain stems nonorthogonal to fold surface. Recently, microfocus (i.e., microbeam) wideangle X-ray diffraction (WAXD) was used to analyze the ringbanded morphology in spherulites.26−28 A single poly(3hydroxybutyrate) (PHB) spherulite has been mapped by means of microbeam X-ray diffraction using a synchrotron source with 7 μm beam,26 and authors concluded that the ringed spherulite of PHB is attributed to the lamellar twisting. Yet, considering the fact that the interband spacing in PHB spherulites is usually 3−10 μm (depending on Tc’s), a synchrotron microbeam of 7 μm diameter might be far from adequacy for analysis as the beam size would cover the entire pitch of twisting. However, later investigators questioned the validity of the continuous twisting model with reservation. Rosenthal et al.,29 in a 2012 revisit to the Keith−Padden’s (K−P) continuous twisting model concluded with frustration that “despite the formal agreement with the K−P model, the value of the chain tilt of 4° does not appear to be sufficient for generation of the surface stresses required for twisted lamellar growth” and proposed “3D-shapes are needed to provide more insights into the nature of chirality of such supramolecular objects formed by Received: March 16, 2018 Revised: May 4, 2018

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achiral polymers.” That is, they on one hand took the model as granted but pointed out the disagreement between the model and results from miscellaneous characterization. In a more recent review article by summarizing many recently studied systems, 28 we have pointed out that the so-assumed continuously helical “chirality” of supramolecular lamellar plates, as the DNA molecule, may not be essential for formation of ring band. That is, lamellae plates in the supramolecular levels can be packed via dramatically different origins, such as patterns seen in various biological grating architects for light diffraction/interference. In a yet more advanced recent study on PTT banding,30 we provided novel views onto the interiors of banded PTT spherulites and revealed a 3D corrugate-board structure with multishell oblate spheroid, where the shell thickness exactly matches with the optical band spacing (ca. 10−15 μm, depending on Tc). Albeit the model of continuous helical twisting had been commonly cited as Keith and Padden’s earlier proposals,12−15 Keith and Padden31 themselves stated emphatically in a 1996 conclusion that even a supposed “unique cause” for twisting orientation in banded polymer spherulites is a chimera meaning creation of imagination. Even though these imagined factors had been assumed repetitively by many investigators for many decades,12−15 Keith and Padden31 themselves had some reservation that they could universally account for ring bands in all polymers. This reservation apparently had been unduly ignored by many later investigators. That is to say, alternative views might be necessary in interpreting the wide variety of banded patterns; in addition, we propose that the lamellar packing in top surfaces of thin films may differ significantly from interiors of thicker polymers as the growth constraints can be completely different. Ring-banded spherulites in poly(1,4butylene adipate) (PBA) and poly(ethylene adipate) (PEA) have attracted attention, and different mechanisms have been examined, as both polymers show apparent extinction doublering bands at a very narrow crystallization temperature range (Tc = 28 ± 3 and 29 ± 2 °C, respectively). PEA’s surface morphological characterization on the ring-banded spherulites of PEA was performed in detail using atomic force microscopy (AFM),32 which revealed that the crystal species on the topsurface bands are discrete and discontinuous with each other. When crystallized at 27−31 °C, PEA is widely known to show vividly alternate banding birefringence on thin-film samples (nanometers to less than 10 μm),33,34 whose ringband mechanism has been widely discussed and was not the objective of this study. To be complete, a recent work35 has cracked open the in-depth mechanisms of periodic banding in PEA via anatomy into interior 3-D lamellae assembly. Such optical patterns in banded PEA spherulites, in polarized optical light, resemble colorful stripes in some insects such as butterflies. That is, biomimetic structures, perhaps in lesser regularity, could possibly be present in the interior crystal assembly of ring-banded polymer spherulites, which are composed by some micro- and nano-ordered lamellae packing in hierarchically repetitive patterns. This study further addressed the details of three-dimensional dissection into interiors of lamellar assembly in spherulites of bulk PEA samples. The orderly assembled lamellae in achieving periodic optical rings in PEA interior assembly is shown to resemble those microstructures in several nature-evolved biological structures for light diffraction.

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Materials and Procedures. Poly(ethylene adipate) (PEA), a lowmelting semicrystalline polyester with Tg = −52 °C and Tm = 43 °C, was purchased as research-grade materials from Aldrich Co. (USA). The weight-average molecular weight (Mw) was nearly 10 000 g/mol, determined by gel-permeation chromatography (GPC, Waters 410) using tetrahydrofuran (THF) as eluent at a flow rate of 1.0 mL/min. The polymer was purified by reprecipitation from chloroform into a cold methanol bath (at ca. −10 °C). For preparation of bulk samples, purified PEA pellets/powders were heated, melted, and then brought to crystallization immediately by quenching into an isothermal plate kept a preset Tc. Alternatively, for preparation of film samples of various thickness, purified PEA was dissolved in CHCl3 (chloroform) in 5−10 wt % concentrations; a few drops were repeatedly deposited on glass substrate to stack into films of thickness in desired ranges. Degassing was performed at 45 °C in a vacuum oven for 24 h. The thickness of dried PEA samples on glass substrates (by subtracting the glass plate) was measured using a thickness probe, with accuracy to ±1 μm. PEA was chosen for study, as it has been known that the crystal morphology of thin-film PEA samples within a narrow Tc (27−30 °C) range displays orderly ring-band patterns.33,34 The details of ring-band patterns and inherent lamellar assembly in PEA banded spherulites, however, might differ from those seen in other ring-banded polymers in that metallic shine and variation of interference colors may be seen in the PEA banded patterns when viewed using optical microscopy. Crystallization conditions are as follows. For comparison of the interior lamellar structures in 3D views, PEA in thick forms (25−50 μm) was typically heated to Tmax = 90 °C, rapidly brought to Tc = 27, 28, 29 °C, etc., held for time = 1 h for full crystallization. For orderly ring bands in PEA, a fixed Tc = 28 °C by quenching from Tmax = 70 °C was used. Note that depending on Tmax for premelting PEA prior to quenching to crystallization, Tc from 29 to 30 °C was also able to produce similarly orderly ring bands in crystallized PEA spherulites, for example, if Tmax was fixed at a higher temperature of 90 °C. During the duration of crystallization, the temperature of the bath was kept exactly isothermal within ±1 °C. As cleavage across a banded PEA spherulite tended to be randomly initiated or located, fracture was performed on crystallized PEA samples several times to acquire sufficient number of specimens for morphology analyses to complete 3D perspectives. Cleavage of PEA spherulites in samples was found to cut through randomly to be sometimes near the poles away from the nuclei and other times across the equator line of spherulites near the nuclei, respectively. Such fracturing provided lateral views in various angles. In yet other fractures that chipped out a piece off the top layer of PEA banded spherulites, the cover surface of banded PEA spherulites was lifted to expose the interiors for top views on their interior lamellae assembly. Statistically together, they provided fuller 3D anatomy. Apparatus. Scanning Electron Microscopy (SEM). Fractured surfaces of bulk-form PEA samples were examined and characterized using scanning electron microscopy (FEI Quanta-400F, SEM) for revealing lamellar structure in the fracture and top free surface of bulk PEA. Samples were coated with gold vapor deposition using vacuum sputtering prior to SEM characterization. Polarized-Light Microscope (POM). Observation of spherulites and patterns of neat PEA was performed in a polarized-light microscope (Nikon Optiphot-2, POL) equipped with Nikon NFX-DX exposure and Nikon NFX-35 CCD digital camera. A λ-tint plate (530 nm) was used in POM. The as-cast neat PEA samples were spread as uniform thin films on glass slides (thickness ca. 10 μm) and dried properly in a temperature-controlled oven before they were examined using the optical microscope. Observation on POM was carried out by heating the sample to a Tmax = 90 °C for 2 min in order to erasing prior thermal histories and then quickly removed to microscopic heating stage preset at a selected temperature of isothermal crystallization. Wide-Angle X-ray Diffraction (WAXD) Measurement. A Rigaku Xray diffractometer, model RINT-TTR III, was used for in situ WAXD measurement with variable temperature settings. The X-ray beam used B

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Macromolecules was Cu Kα radiation (λ = 0.154 nm), in powder-pattern mode, measured in the 2θ range of 15°−30°, and the heating rate was set at 1 °C/min. Use of this instrument to perform characterization on PEA was a courtesy granted by Prof. K. Tashiro of Department of Future Industry-oriented Basic Science and Materials, Toyota Technological Institute, Nagoya, Japan, while coauthor Kai-Cheng Yen was a visiting student/exchange scholar to Prof. Tashiro’s lab. Small-Angle X-ray Scattering (SAXS) Measurement. A Rigaku Nanoviewer high brilliant small-angle X-ray scattering (SAXS) system was used for small-angle measurement, which is equipped with a Rigaku Dectris detector (Pilatus) for recording the scattering signals. The X-ray beam used was Cu Kα radiation (λ = 0.1542 nm). The Xray powder patterns were measured in the small 2θ range of 0.15°− 1.2°. The scattering intensity I(q) was transformed to I(q)q2 for the correction of Lorentz factor, where q is a scattering vector defined as q = (4π/λ) sin(θ), where λ is wavelength of incident X-ray beam and 2θ is scattering angle. Use of SAXS instrument to perform characterization on PEA samples was a courtesy granted by Prof. K. Tashiro. SAXS measurements were performed for revealing the lamellar structures of banded vs nonbanded PEA.

morphology clarity, we characterized using SEM, instead of POM, on banded PEA spherulites (after acetone etching) in an extremely thick (ca. ∼500 μm) bulk sample, whose result is shown in Figure 1d. Apparently, the banding pattern and interband spacing in the SEM micrograph for such extremely thick bulk PEA films are the same as those in thinner PEA films. To understand fully the mechanisms of regular banding in spherulites, the interior lamellae, and not just the top-surface crystals in crystallized films, should be sufficiently examined in all directions. Top-view analysis (by fracturing parallel to top surface) on internal lamellae of PEA banded spherulites was first attempted. In addition to the cross thickness-fractured samples, fracturing was performed so that the top surface (where alternating circular rings were located) was removed parallel to the top surface. Propagation of fracturing was controlled so that in one PEA sample (Tc = 28 °C) the fracture was oriented to be parallel and perpendicular to top surface, respectively. Like the SEM results discussed earlier on samples where thickness was cross-fractured in PEA samples, this time the PEA samples were specifically fractured along the parallel top surface where conventional ring bands patterns are located, like in a surgery where the lid of skull was lifted up so that internal brain tissues could be inspected. SEM characterization was performed on the top-surface lifted and thickness-fractured PEA samples. Resemblance to Structured Biology Systems. Lamellar assembly is reflected in the optical birefringence patterns in PEA spherulites. Figure 2 shows top surface-relief morphology

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RESULTS AND DISCUSSION Periodic Bands and Birefringence Patterns. Figure 1 shows POM graphs of PEA films of increasing thickness (10−

Figure 1. POM micrographs for banded PEA spherulites in film samples of increasing thickness (a−c for 10, 20, and 30 μm, respectively). (d) SEM micrograph for banded PEA spherulites in 500 μm thick bulk film. Tc = 28 °C for all samples. Ring-band patterns are preserved with same interband spacing in PEA samples of all film thickness.

50 μm), all crystallized at the same Tc = 28 °C. Other than the retardation/birefringence difference (owing to different thickness), the ring-band patterns in PEA samples of various film thickness remain much the same, with same inter-ring spacing (∼7 μm). This fact proves that the ring-band birefringence patterns and characteristic inter-ring spacing in PEA spherulites crystallized at Tc = 28 °C are not altered by film thickness; thus, the optical birefringence patterns in ring-banded spherulites in thinner PEA films could be meaningfully compared and correlated to the crystal assembly in thicker/bulkier PEA banded ones. POM micrographs for thicker PEA film samples (50 μm) still display similarly visible banding pattern with the interband spacing being the same as those in thinner PEA films. Note that with increasing film thickness the polarized optical light cannot fully penetrate through thick films to yield wellresolved morphology for banding patterns. Thus, for better

Figure 2. Surface-relief morphology (SEM micrographs) of PEA banded spherulites (Tc = 28 °C) in samples: (a) before acetoneetching and (b−d) after acetone etching at increasing magnifications.

of PEA spherulites before and after acetone etching for further exposing the inner lamellae hidden underneath the periodic rings. The seemingly continuous ring bands on top surface of spherulites, when solvent-etched, display that the bands are composed of discrete arrays of lamellar skeletons that are aligned as multiple rings with inter-ring spacing = 7 μm. The individually bundled lamellae skeletons on the ridge are roughly 200−500 nm in diameter and ca. 3 μm in length. Note that the magnified SEM micrograph reveals that the acetone etching on banded spherulites properly exposes the circular ridge bands to be composed of nearly parallel-aligned and pyramid-shaped slits C

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with alternating ridge-rib corrugate-board structures. Note the striking similarity in both dimensions and shapes of the PEA microcrystals and butterfly wing scales. The interior of PEA banded spherulites might differ in minute details from those in the wing scales; however, the main features are similar. The PEA spherulite lamellae are apparently assembled into a corrugate-board structure that is almost identical to those in the butterfly wing, except that the liner (also called “ridge”, the interface between the successive flute layers) in the wing scale is straight while that in the PEA spherulites is arc-shaped. The dimensions of the microstructures in the PEA banded spherulites and butterfly wings are compared as following. The SEM micrograph in this figure clearly shows the interior crystal assembly in the ring-banded PEA spherulites is apparently structured as corrugate-board liner and flute medium resembling latticed gratings, which is mimetic with the micro/nano-architectures of biological wings/feathers for diffracting optical light into colors. Crystals of regular repetitive optical patterns, such as the ring bands in PEA spherulites, require some hierarchical orders, which resemble those in biostructured colors. It has also been well documented that the metallic shines and color changes in some biology systems as viewed from different angles may come from structured orders in the wing scales that cause refraction of light with different wavelengths. This takes hierarchically structured assembly in micro- to nano-orders, and the most notable example is from the structured blue colors of a morpho butterfly wing. Thus, the scales from nano- to microhierarchical packings in some biology systems are found to be similar to the layered assembly of interior lamellae in banded PEA spherulites. For the peacock, as many birds, the plumage colors of its feather are known to be not due to pigments, but optical interference reflections,36 which are based on genetically governed regularly periodic micro- or nanostructures of fibrillar arrays of the barbules in a feather. Changes to the spacing (or optical light beam angle) of these structures result in different combination of colors in interference with sunlight. Such periodic structures with microor nanostructures in a birds’ feather are now proven to be a similar mimic to those in the periodically banded PEA spherulites. The dimensions and interslit spacing quite resemble those counterparts in typical butterfly wing scales that have been addressed in many biostructure-related studies.36−39,41−43 By eliminating the minute differences of SEM images reported among various investigators,36−39 the main features of butterfly wings for light diffraction are shown here as a summary schematic plot in Figure 3B. The interslit spacing in a butterfly’s wing is ca. 200−250 nm; by comparison, the interlamellae spacing (PEA etched) on the ridge is ca. 300−500 nm. The corrugate-board structure in butterfly wings has an inter-ridge spacing = 3.5 μm, and the interslit spacing is ca. 0.2 μm apart. By comparison, the PEA ring band has an inter-ring = 7 μm, and the interkebab spacing (the ribs) varies between ca. 0.5 and 2 μm (not regularly uniform owing to random fracturing). The inter-ring spacing (7 μm) in PEA spherulites perfectly matches with the optical banding seen in POM graphs, while the interslit spacing matches with the interfibrillar voids seen on the top surface (shown earlier in Figure 2). The interslit in PEA spherulites is not so uniformly spaced, which can be attributed to solvent etching or mechanical stress used in fracturing the spherulites apart for SEM characterization. By contrast, the blue morpho butterfly wing has a quite constant interslit spacing to be ca. 0.2 μm (∼220 nm), which is the half-wavelength of blue

that run in the radial direction. Such discrete structures on topsurface morphology suggest that the interior lamellae are similarly assembled to be discontinuous. The above discussion is confined only to the top-surface relief morphology of periodic banding; however, a more essential feature of lamellar assembly of banded PEA spherulites in interiors is needed for fuller scopes. In a previous study,35 we have amply proved that the top surface of PEA ring-banded samples exhibits protruded pyramidal-shaped crystals that correspond to the ridge bands. The pyramid protrusion crystals are aligned along the ridge bands. By contrast, the valleys of the top surface are covered or filled to form a flat band. Sample fracturing was attempted to expose the interior assembly, and fracturing of thick-bulk PEA films further exposed the interiors to allow better analyses on the lamellae morphology with anatomy views in the ridges and valleys, respectively. The threedimensional lamellae in the ring-banded PEA spherulites apparently are composed of successive corrugate-board patterns (i.e., orderly grating structures), which eventually appear as alternating ridges and valleys of ring bands as they reach the outer top surfaces. Each of the interior lamellar plates on the ridge band is visibly bent to a curvature. The interspacing and width of the periodically corrugate-like PEA bands measured using SEM are nearly 6.5−7.0 μm, which are in full agreement with the quantities of inter-ring spacings measured by independently separate AFM and/or POM characterizations. We will draw attention to the striking similarity in the corrugate-board assembly of PEA crystals to the blue morpho butterfly’s wings with orderly gratings in microscopic structures. More specifically, the specific genus of morpho butterfly wings,36−39 with shining blue color, is used for producing the schematic drawing of orderly grated slits on the scales. Figure 3A,B shows SEM micrographs for the interior lamellae

Figure 3. (A, B) PEA orderly ring bands as viewed in SEM graphs (reproduced with permission from ref 40) in comparison to (C) summary scheme of orderly aligned scales in morpho butterfly wings.

structures in the orderly circular bands of PEA spherulites.40 Note that graphs A and B are SEM morphology results on a same specimen taken from slightly different electron-beam angles; however, common traits of grating assembly of interior lamellae are apparent in the ringed PEA spherulites. Corresponding POM micrographs of PEA thin films have been verified to display vividly periodic blue/orange ringed birefringence alteration.40 Figure 3C shows a comparison of orderly lamellae of the PEA ringed spherulites to a generalized schematic drawing of the orderly aligned scales in a morpho butterfly wing as reported in numerous related studies on biostructural coloration.36−39,41−43 The anatomy of morpho butterfly wings, when magnified as shown in the schematic, shows roof-tile packing of scales, where the scales are covered D

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ular to the board shells exposing the U-shaped crystal plates and (region II) morphology parallel to the board shells exposing the intershell cilia lamellae. This nearly 3D fracturedinterior morphology in the ringed PEA spherulites shown in this figure is critically valuable to answer an important issue that is long debated: whether or not the interior lamellar plates of ring-banded polymer spherulites rotate continuously in a helixtwist fashion. From the top-surface ring bands (bottom half of the SEM graph), the grating slit thickness is ca. 6−7 μm (interring spacing). It is clear that the alternating ring bands on top surface correspond to the interior alternating lamellar plates underneath the top surface. The thickness of each of the lamellar plates in the 3D interior is roughly 6−7 μm, which is exactly the same as the inter-ring spacing on the top surface. There are five grating shells in interiors, and correspondingly there are five bands on top surface of the ringed PEA spherulites, where the cilia lamellae are located exactly underneath the top-surface ridge band and the interior Ushaped plates are situated underneath the valley band on top surface. Without lifting the top layer of ringed PEA spherulites to expose the interiors, such 3D lamellae assembly leading to periodic ringed spherulites and the hidden grating structures for optical birefringence pattern could never be realized and proved. Once again, correlations between the top-surface ring bands and interior corrugate shell-layered lamellae and their orientations have revealed one critical morphology feature leading to fuller understanding of the lamellae assembly mechanisms responsible for periodic optical patterns in polymer spherulites. Thus, the SEM characterization on dissected interiors of ring-banded PEA samples clearly reveals that these cilia lamellae (intershell) or U-shaped plates (the shells) never make a continuously full helicoid-turn twist. The interior Ushaped plates (radially oriented) do twist randomly, owing to interfacing and/or impinging with the cilia lamellae (tangentially oriented). Note that the perpendicular lamellae are composed of inverted “U”-shaped crystals; by contrast, the shell-sandwiched interlayers are composed of cilia crystals that assume completely different geometry and orientations from those of the U-shaped crystal plates. Apparently, it is the alternating lamellar-bundle shells of distinctly different orientations/geometry underneath the top surface that cause the alternating ring bands on the top surface. All lamellar plates, with occasional localized bending/twisting, are roughly perpendicular to the top surface. After examining the interiors from the cross thickness vs parallel to top surface of interior crystal assembly in PEA ring banded spherulites, the inter-relation between the crystal species of ridge vs valley bands is further established with a closer analysis. For a closer-up top view into the interior of a banded PEA spherulite, Figure 5A shows a much higher magnified SEM graph (6000×) revealing the perpendicular lamellar plates of 5 μm thick and thin sandwiched interlayers (1 μm thick) in bulk PEA film crystallized at 28 °C. Figure 5B shows a schematic plot according to the SEM-revealed interior lamellar assembly in the ringed PEA spherulites. The interior corrugate-board structure (scales in order of magnitude as those micro/nano-structures in butterfly wings) packed of interlined lamellar plates. The liner crystals (tangential oriented) and U-bent and fish-scale-like crystals (radial oriented) intersect at two mutually perpendicular orientations. The dimensions for the grating structure are roughly flute (Ushaped shell) = 6 μm plus the liner layer = 1 μm. Apparently,

light (440 nm). Other interslit spacing in wings of various butterfly species might be genetically structured for diffracting into different colors of iridescence. In plants, insects, or animals, iridescence is generated by the interaction of light with biological tissues or features that are nanostructured or microstructured into hierarchical scale-like or layer-like patterns to produce either antifouling properties44 or diffraction gratings for colors.36−39,41−43 In addition to structured colors, many other biostructures have been used by animals for miscellaneous purposes. The goose down feather has a fractal treecanopy-like structure for insulation purposes, but it has no periodic orderly slits for diffraction; thus, only diffused scattering to white color results, which is correspondingly different from those in the colorful peacock feather barbules or butterfly wings. It then became essential that fracturing in various planes of PEA samples should be attempted so that morphology in fracture lines parallel and across the valley/ridge bands could be observed. SEM characterizations were conducted in series on several different fractured samples to search for such evidence. Figure 4A,B shows SEM micrographs for the fractured interiors

Figure 4. SEM graphs exposing the fractured interiors: (A) through thickness vs (B) parallel to top surface in ringed PEA crystallized at 28 °C. Fracture lines were perpendicular and parallel interior corrugate board shells, respectively.

of periodically banded PEA spherulites, revealing a 3D interior morphology of a corrugate-board structure with alternating board shells underneath the top-surface bands. Figure 4A shows the fractured surfaces in the lateral side (thru the film thickness) in correlation with the fractured surface parallel to top-surface of the crystallized PEA films. The fact that the board shells are exposed in both fractured surfaces (thru film thickness and parallel to top surface of films) suggests that the grating board shell structures are in the 3D spherulites and not just in one dimension. Figure 4B shows that two dramatically different crystal species (differing in crystal/lamella shapes) can be identified in exposed PEA spherulites from the SEM micrographs: (region I) morphology by fracturing perpendicE

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lattices and these effects are not specific only to PEA but are characteristics of ringed spherulites of polymers and other materials. Yet, Point at that time did not have a chance to experimentally investigate the top surface versus the interiors of ring-banded PEA spherulites. Thus, the grating-latticed structures as exemplified in this work for the ringed PEA spherulites can possibly behave like the gratings in peacock feather barbule crystals or butterfly wings.36−39 Those earlier theoretical proposals by Point a decade ago are now clearly and experimentally supported by this work via dissection into interiors to expose the hidden 3D crystal assembly in the banded PEA spherulites, whose crystal assembly demonstrates close biomimetic similarity to the well-studied biological grating structures for optical light iridescence into colors. Top Surface Relief Morphology versus Interior Assembly. The outer top-surface morphology can differ subtly from the interiors of ringed polymer spherulites; thus, a description of the assembly mechanism cannot be complete without correlating these two morphologies (top-surface reliefs vs interiors), which might differ but correlate with each other in subtle ways. Figure 6 shows (A) SEM micrographs the top-

Figure 5. (A) Zoom-in SEM graph (6000×) and (B) 3D scheme for interior grating structure, revealing the perpendicular lamellar plates and sandwiched interlayers in banded PEA spherulites crystallized at Tc = 28 °C.

the lamellar plates are perpendicular to the top surface, but they are roughly parallel to each other, arranged orderly. The lamellar plates are composed of inverted “U”-shaped crystals from top view (but rectangle from side view when fractured across the film thickness), and each of the U-shaped crystals appears to be horizontally stacked within the vertical plates. One can see some of the ends of U-shaped crystals in the perpendicular plates may taper to bend 90° and finally thin out into the shell-surface regions to become cilia crystals. The fluteliner corrugate structure of interior of the banded PEA spherulites is similar in dimensions and geometry to the assembly in the biophotonic crystals of peacock barbules, in which Kinoshita et al.36 in a study on physics of photonic structures have examined the interior assembly of peacock feather (Indian peafowl) using SEM (see Figure 24b of ref 36). The comparisons demonstrate that the crystal assembly of periodicity shares some fundamental striking similarity. Note that although the cilia-like crystals (shish lamellae) and U-shaped plates (kebab lamellae) are connected, there is a distinct discontinuous interface between them, which accounts for the clean and easy cleavage between the ridge and valley band. The fact that the cilia-shell surface was cleanly fractured away from the U-shaped plates to expose the individual lamellar plates indicates that there is little entanglement between the cilia fibrous lamellae and the U-shaped lamellar plates. That is, the crystals in the U-shaped plates are of a different orientation from that of the cilia interlayers. The interboard surfaces are composed of much thinner crystals (i.e., cilia lamellae) that are oriented vertically and pointing toward the top surface. That is, the sandwiched shell surface crystals are much thinner and oriented differently from the U-shaped stacked lamellae. The width of the cilia shell plus U-shaped stacked lamellae underneath the top surface is equal to 6 μm, which coincides with the inter-ring spacing distance of ring bands seen on the top surface. Thus, the dissected interiors of PEA with orderly periodic bands are shown in this work to appear and function similarly as optical diffraction gratings in some biological species. In studying the optical polarized-light birefringence of PEA, Point45,46 in 1953 pointed out that the transmittivity of light intensity through spherulitic films of ring-banded poly(ethylene adipate) (PEA) is not uniform across the spherulite. Later in more extensive analyses via theoretical calculations and modeling, Point47 in 2006 further inferred that the crystallized ring-banded PEA films could possibly function as grating

Figure 6. SEM micrographs for correlation between (A) the topsurface relief patterns and (B) interior grate-terrace structure, both displaying a board thickness ca. 7 μm (= optical band spacing).

surface relief patterns in correlating to (B) the interior grating structure of PEA banded spherulites (Tc = 28 °C). Note that fracture into interior was statistically random; thus, the exposed morphology could differ slightly depending on locations. However, the interiors of banded spherulites are invariably and similarly grating-structured. Both top-surface periodic rings and interior corrugate board display an interspacing thickness equal to ca. 7 μm. This is exactly the inter-ring spacing (7 μm) in POM micrographs shown earlier in Figure 1. The close matching in these dimensions of optical feature and interior lamellae suggests strongly that the boarded structure is responsible for the periodically optical rings. The interior boards show a finely grated structure where the kebab-like crystals are in the radial direction and the cilia crystals run in the liner direction (i.e., tangential direction). As the interior of PEA samples was not acetone-solvent-etched as the top-surface relief PEA samples, the grated structures in interiors of PEA spherulites are not as obvious as those in the solvent-etched top surface patterns. In addition, the hairy-cilia protrusion (refer to earlier Figure 2) on the ridge of solvent-etched PEA spherulites is similar to the microscale bumps on a lotus leaf48 or for intensifying the light diffraction on firefly,49 except that the bumps on the lotus leaf or firefly are evolution-spaced and not aligned on a ring. The bumps on the lotus leaf are also taller (5−10 μm) than those on the PEA banded spherulites. It is worthy to note that the terrace-layered structure of interior of F

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coincidence, but more likely related to nature’s ways of assembling into hierarchical orders. It is worthy to note here that a similar shish-kebab structure (with the crystallographic orientations between the kebab and shish crystals being identical) in thin-film (for TEM) isotactic polypropylene (iPP) was reported by Yan et al.,51 where they claimed that highly lamellar branching of α-form iPP constitutes the “kebab” lamellae. The grating structure in ringed PEA is also similar to the PE’s shish-kebab structure reported earlier by Lovinger et al.,52 Varga,53 or Pennings and Kiel.54 It should be noted here that albeit the grating-structured morphology (shish-kebab structure similar to that in the pollia berry as illustrated in scheme of Figure 7) is apparently present in thin-flim iPP,51 no ring-banded birefringence is ever reported for iPP, perhaps owing to the fact that its hierarchical lamellar structures at greater film thickness (for POM characterization) may differ significantly from that at ultrathin film state suitable for TEM characterization. Crystal Lattice Forms and Lamellar Thickness Distribution. Some might question whether the polymorphism and crystal lattices in PEA spherulites could influence the lamellar assembly into periodic patterns. To address it more thoroughly, the crystal lattices in PEA at various Tc’s were examined using X-rays. Figure 8 shows temperature-dependent

PEA banded spherulites is apparently similar to the biophotonic crystal assembly in peacock feather barbules.36 Figure 7 shows SEM micrographs for two different portions of the interiors (fractured) of a PEA banded spherulite of

Figure 7. (A) SEM micrographs for interior grating-boarded structure of PEA banded spherulites in comparison to (B) skin of Pollia fruit with vivid blue color owing to strong diffraction of light in ∼440 nm wavelength.50

another PEA sample crystallized at Tc = 28 °C. Fracturing across the interiors of PEA samples was statistically random across various portions of a spherulite, and thus the exposed morphology might differ slightly for different PEA samples. These two SEM graphs were obtained by focusing on two outer portions of the spherulites; thus, the flute plates and liner ridges (protruded tangential crystals) appear to be straight and less arc-shaped. Nevertheless, the main feature remains the same, which is a grate-structure-like assembly resembling the butterfly wings discussed earlier. The corrugate-board assembly (SEM graphs on top) of PEA banded spherulites is composed of multiple flutes with the straight liners (acting as shish lamellae) intersecting almost perpendicularly with U-shaped kebab lamellae. The nano- to microscale voids between the kebab lamellae suggest that the kebab lamellae are distinctly stacked at a normal direction to the interflute liners. More astonishingly, as one compares this unique morphology in the banded PEA spherulites to the magnified skins of Pollia-berry fruits,50 Pollia condensata, also called the marble berry, the similarity between the PEA crystal assembly and the bioiridescence structure is also striking. Figure 7B shows schematic plot of the Pollia-berry skin, via hierarchical cellulose crystals, which assembles into an orderly grating structure for diffracting blue light. By close similarity, the PEA lamellae (at Tc = 28 °C) assemble themselves into an orderly gratings for achieving periodic birefringence ring patterns. Apparently, the interior anatomy of 3D lamellae assembly of PEA periodical banded spherulites can be mimetically compared to the biostructures for specific optical iridescence. Similarity in the orderly grating structures is shared between the PEA banded spherulites and the biostructural orders for light interference through detailed comparisons to the morpho butterfly’s wing, the microscopic crystals of peacock’s feather barbules, and the microscopically structured surfaces composed of hierarchical cellulose crystals in Pollia fruit’s skin. All cases demonstrate striking similarity between the interiors of PEA banded corrugate-board array with those bioevolved structures for optical purposes. Thus, the similarity of the PEA periodically crystal assembly and the biostructures of three different biospecies is not to be regarded as just incidental

Figure 8. Temperature-dependent WAXD results for PEA samples initially crystallized at Tc = 28 °C and then gradually heated to 70 °C. Insets: corresponding POM graphs for 28 °C crystallized PEA samples, then heated back to the respective temperatures as indicated.

WAXD results for PEA ring-banded spherulites initially meltcrystallized at Tc = 28 °C and then gradually heated to 70 °C in situ on a temperature-program cell. Corresponding POM graphs at various Tc’s are attached for showing gradual melting of lamellae in ring-banded PEA spherulites at increasing temperature from 28 to 70 °C. The POM graphs show that the ring-banded patterns remain intact upon heating from 28 to 51 °C. Note here, though, the PEA samples for POM characterization were cast on glass slides while for WAXD characterization, samples were PEA films placed on an aluminum stand (for powder patterns). Nevertheless, the thermal schemes imposed on both sample sets were closely G

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Macromolecules comparable. A minor amount of meta-crystal modification (termed here as “β”) is initially present in 28 °C crystallized PEA (ring-banded) at 2θ = 21°. With in situ heating from 28 to 51 °C, the meta-crystal modification disappears with a corresponding increase of intensity at 2θ = 21.5° (110); nevertheless, the birefringence patterns remain to be ringbanded between 28 and 51 °C. The fact suggests that the minor amount of meta-crystal modification form (β-form) formed at Tc = 28 °C is not a prerequisite condition for formation of ring bands in crystallized PEA. This meta-form lattice quickly transforms into a more stable form upon heating, without influencing the corrugate-board lamellae shapes that have been already packed into ring-banded spherulites. For comparison between the PEA crystals in spherulites generated from melt crystallization versus cold crystallization, Figure 9 shows WAXD results and corresponding POM graphs

Figure 10. SAXS profiles of PEA crystallized at Tc = 28 °C (ringbanded) vs Tc = 35 °C (ringless).

Figure 9. X-ray diffractions for cold-crystallized PEA at Tcc = 20, 25, 28, and 35 °C. Inset: POM graph for corresponding birefringence patterns (ringless) at Tc = 20 °C.

the thickness distribution of lamellae does not differ much between these two types. Note that the individual lamellar thickness normally increases slightly with respect to increase in Tc (28 vs 35 °C). The difference of lamellar thickness, however, is not much, suggesting that the ordered grating-like structure in the ring-banded PEA spherulites is packed by hierarchical structure levels much above the 10−15 nm scales of individual lamellae thickness. The corrugate-board structures in the ringbanded assembly of PEA spherulites are likely in ranges of 200 nm to a few micrometers of aggregated lamellar bundles, as demonstrated in the earlier SEM micrographs. The assembly differences in the banded vs ringless structures cannot not be possibly detectable by regular SAXS analysis. Collectively, the WAXD and SAXS results can be used as clear supporting evidence that the individual lamellae thickness and crystal lattices do not change between the banded vs nonbanded crystal aggregations. Only the bundled lamellae assemble themselves in different ways.

for PEA spherulites cold-crystallized at Tcc = 20, 25, 28, and 35 °C, in contrast to the earlier results from melt crystallization. Apparently, the spherulites of cold-crystallized PEA are all tiny and ringless at Tc = 20−35 °C; the WAXD data show that all cold-crystallized PEA samples have identical diffraction peaks for (111), (110), and (020) planes, with no meta-crystal form at 2θ = 21°. However, it should also be emphasized here that the presence of meta-crystal form at 2θ = 21° is not necessarily associated with the ring bands, as the results in the previous figure already prove that the transformation and disappearance of the meta-crystal form at 2θ = 21° upon heating does not influence the ring-band patterns. The X-ray results in this figure further prove that regardless of PEA lamellae being assembled into ring bands or not, the crystal lattices remain the same. Furthermore, in a previous publication,35 we suggested that the meta-form likely might be part of the hierarchical ring-band structure (in the cilia-like tangential crystals). This meta-form may accompany the formation of ring bands in PEA crystallized at Tc = 28 °C, but its disappearance and transformation into the stable crystal lattice upon heating do not influence the ring bands. The lamellae thickness of PEA crystallized into ring-banded (Tc = 28 °C) vs ringless (Tc = 35 °C) spherulites is compared in Figure 10. The SAXS data for these two types of PEA spherulites (ring-banded vs ringless) indicate that the lamellar thickness/distribution of ring-banded PEA spherulite at Tc = 28 °C is a bit smaller than that of ringless one at Tc = 35 °C, but

CONCLUSION The half-century long debates on mechanisms of periodic bands in polymer crystals reflect that there had been an overwhelmingly insufficient understanding of the true mechanisms that direct, control, and fine-tune the formation of these repetitively periodic micro- to nanostructures for visual optical banding. This work further shows that the dissected interiors of banded PEA spherulites closely resemble those in some natural structured colorationboth are based on periodic algorithm of gratings for developing ordered structures with micro- and nanometer hierarchical scales. Nevertheless, there are some subtle differences between the banded PEA crystals and natural biological photonic crystals. In this work, the interior anatomy of 3D lamellae assembly of PEA periodical banded spherulites is delicately and mimetically compared to the biostructures for specific light iridescence. Not only comparisons are done to the blue morpho butterfly’s wing but also to the microscopic crystals of peacock’s feather barbules. Comparison is also done to the Pollia fruit, with striking similarity between the PEA banded corrugate-board array and the Pollia fruit’s skin possessing microscopically structured surfaces composed of hierarchical cellulose crystals for light interference. Thus, the similarity of the PEA periodically crystal assembly and biostructures of three different biospecies is not to be regarded as just an incidental coincidence. An additional objective accomplished in this work is to furnish critical experimental results to Point’s

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their cyclodextrin inclusion complexes. Biomacromolecules 2003, 4 (3), 783−792. (3) Gan, Z.; Abe, H.; Kurokawa, H.; Doi, Y. Solid-state microstructures, thermal properties, and crystallization of biodegradable poly(butylene succinate)(PBS) and its copolyesters. Biomacromolecules 2001, 2 (2), 605−613. (4) Kuwabara, K.; Gan, Z.; Nakamura, T.; Abe, H.; Doi, Y. Molecular mobility and phase structure of biodegradable poly(butylene succinate) and poly(butylene succinate-co-butylene adipate). Biomacromolecules 2002, 3 (5), 1095−1100. (5) Gan, Z.; Abe, H.; Doi, Y. Crystallization, melting, and enzymatic degradation of biodegradable poly(butylene succinate-co-14 mol ethylene succinate) copolyester. Biomacromolecules 2001, 2 (1), 313−321. (6) Hao, Q.; Li, F.; Li, Q.; Li, Y.; Jia, L.; Yang, J.; Fang, Q.; Cao, A. Preparation and crystallization kinetics of new structurally well-defined star-shaped biodegradable poly(L-lactide) s initiated with diverse natural sugar alcohols. Biomacromolecules 2005, 6 (4), 2236−2247. (7) Mincheva, R.; Delangre, A.; Raquez, J.-M.; Narayan, R.; Dubois, P. Biobased polyesters with composition-dependent thermomechanical properties: synthesis and characterization of poly(butylene succinate-co-butylene azelate). Biomacromolecules 2013, 14 (3), 890− 899. (8) Teramoto, Y.; Nishio, Y. Biodegradable cellulose diacetate-g raftpoly(l-lactide) s: thermal treatment effect on the development of supramolecular structures. Biomacromolecules 2004, 5 (2), 397−406. (9) Cranston, E.; Kawada, J.; Raymond, S.; Morin, F. G.; Marchessault, R. H. Cocrystallization model for synthetic biodegradable poly(butylene adipate-co-butylene terephthalate). Biomacromolecules 2003, 4 (4), 995−999. (10) Haynes, D.; Abayasinghe, N. K.; Harrison, G. M.; Burg, K. J.; Smith, D. W. In situ copolyesters containing poly(L-lactide) and poly(hydroxyalkanoate) units. Biomacromolecules 2007, 8 (4), 1131− 1137. (11) Gestí, S.; Almontassir, A.; Casas, M. T.; Puiggalí, J. Crystalline structure of poly(hexamethylene adipate). Study on the morphology and the enzymatic degradation of single crystals. Biomacromolecules 2006, 7 (3), 799−808. (12) Keith, H.; Padden, F. The optical behavior of spherulites in crystalline polymers. Part I. Calculation of theoretical extinction patterns in spherulites with twisting crystalline orientation. J. Polym. Sci. 1959, 39 (135), 101−122. (13) Keith, H.; Padden, F. The optical behavior of spherulites in crystalline polymers. Part II. The growth and structure of the spherulites. J. Polym. Sci. 1959, 39 (135), 123−138. (14) Keller, A. Investigations on banded spherulites. J. Polym. Sci. 1959, 39 (135), 151−173. (15) Keith, H.; Padden, F. Twisting orientation and the role of transient states in polymer crystallization. Polymer 1984, 25 (1), 28− 42. (16) Lustiger, A.; Lotz, B.; Duff, T. The morphology of the spherulitic surface in polyethylene. J. Polym. Sci., Part B: Polym. Phys. 1989, 27 (3), 561−579. (17) Toda, A.; Arita, T.; Hikosaka, M. Three-dimensional morphology of PVDF single crystals forming banded spherulites. Polymer 2001, 42 (5), 2223−2233. (18) Bassett, D. Polymer spherulites: a modern assessment. J. Macromol. Sci., Part B: Phys. 2003, 42 (2), 227−256. (19) Bassett, D.; Hodge, A. In On the morphology of melt-crystallized polyethylene I. Lamellar profiles, Proceedings of the Royal Society of London A: Mathematical, Physical and Engineering Sciences, 1981; The Royal Society: 1981; pp 25−37. (20) Bassett, D.; Hodge, A.; Olley, R. In On the morphology of meltcrystallized polyethylene II. Lamellae and their crystallization conditions, Proceedings of the Royal Society of London A: Mathematical, Physical and Engineering Sciences, 1981; The Royal Society: 1981; pp 39−60. (21) Schultz, J. M. Self-induced field model for crystal twisting in spherulites. Polymer 2003, 44 (2), 433−441.

theoretical analysis, who inferred in 2006 that the crystallized ring-banded PEA films could possibly function as grating lattices and these effects are not only specific to PEA but are characteristics of ringed spherulites of other polymers. This work has provided essential experimental data and analyses by comparing the PEA band’s 3D interior assembly with several nature’s microscopic grating structures. The 3D nature of the biological microstructures is so much more complex, in comparison to the dramatically simpler periodic pattern with a regular geometry in PEA banded spherulites. The PEA banded spherulites are not a living organism; thus, the periodic arrays of micrometer layers and nanometer lamellae are fixed and controlled by crystallization kinetics of growth; by contrast, the natural photonic crystals are involved in million-year continuous evolution for suitable colorgenerating structures and are much more highly optimized and ordered for light interferences. We do not attempt to draw analogy between the crystal assembly in periodically banded PEA spherulites to the complex biologically evolved structures for light iridescence; yet, there is interesting similarity in the interior corrugate-board structure assembly and top-surface bumped ridge arrays in PEA banded spherulites does exist when compared to some biological structures for specific photonic functions. Via these comparisons of the nature’s assembly of biological photonic crystals or microscopic biostructures, a novel view on mechanisms of polymer crystals into periodic banding birefringence is established to a fuller extent.

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AUTHOR INFORMATION

Corresponding Author

*(E.M.W.) E-mail [email protected]; Fax +886 6 2344496, Tel +886 6 275-7575 ext 62670. ORCID

E. M. Woo: 0000-0002-3653-2549 Present Address

K.-C.Y.: Formosa Plastics Corporation, 201, Tung Hwa N. Road, Taipei, Taiwan. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work has been financially supported by a basic research grant (MOST 105-2221-E-006-246-MY3) for three consecutive years from Taiwan Ministry of Science and Technology (MOST), to which the authors express their gratitude. A portion of the data (WAXD and SAXS) were obtained while coauthor K. C. Yen did a short-term visit/training with Prof. Kohji Tashiro’s laboratory at Department of Future Industryoriented Basic Science and Materials, Toyota Technological Institute, Nagoya, Japan, to whom authors expressed gratitude for hosting and training her hands-on experiences as part of her doctoral program at NCKU as well as courtesy granted by Prof. K. Tashiro for using WAXD and SAXS instrument to perform characterization on PEA.

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