Abstract
Gracillariidae, the family to which Epicephala belongs, is a large group of miniature moths with roughly 100 recognized genera and 2000 recognized species (De Prins and De Prins 2016). They have a global distribution and are found almost everywhere there are plants, except for extremely harsh environments (e.g., the arctic). Gracillariidae is one of several lepidopteran families that consist almost entirely of leaf-mining species, although the leaf-mining habit itself is known to occur in about 30 moth families (Powell et al. 1999). In most gracillariid species, early-instar larvae have remarkably flat head capsules without chewing mandibles, and feed exclusively on cell sap within the nongreen, epidermal layer of the leaf (sap feeder; Fig. 5.1). Later-instar larvae then feed on the palisade layer and finally the spongy layer of the leaf with functional mandibles, and excrete granular frass (tissue feeder; Fig. 5.1). The larvae of the genus Phyllocnistis are exceptional in that they spend all their instars as sap feeders in the leaf epidermal layer. Gracillariid moths are thus unique among insects in that they undergo hypermetamorphosis, a process by which some larval instars become functionally and morphologically distinct from other instars.
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Keywords
- Active Pollination
- Epicephala
- Gracillariidae
- Flueggea
- Glochidion
- Ornixolinae
- Phyllanthus
- Phylogeny
- Proboscis
- Seed parasite
1 Diversity and Classification of Gracillariidae
Gracillariidae , the family to which Epicephala belongs, is a large group of miniature moths with roughly 100 recognized genera and 2000 recognized species (De Prins and De Prins 2016). They have a global distribution and are found almost everywhere there are plants, except for extremely harsh environments (e.g., the arctic). Gracillariidae is one of several lepidopteran families that consist almost entirely of leaf-mining species, although the leaf-mining habit itself is known to occur in about 30 moth families (Powell et al. 1999). In most gracillariid species, early-instar larvae have remarkably flat head capsules without chewing mandibles, and feed exclusively on cell sap within the nongreen, epidermal layer of the leaf (sap feeder ; Fig. 5.1). Later-instar larvae then feed on the palisade layer and finally the spongy layer of the leaf with functional mandibles, and excrete granular frass (tissue feeder ; Fig. 5.1). The larvae of the genus Phyllocnistis are exceptional in that they spend all their instars as sap feeders in the leaf epidermal layer. Gracillariid moths are thus unique among insects in that they undergo hypermetamorphosis , a process by which some larval instars become functionally and morphologically distinct from other instars.
Sap feeding is an apomorphy among Gracillariidae that clearly distinguishes them behaviorally from other leaf-mining Lepidoptera . The extent to which their evolutionary success has been facilitated by sap feeding is a fascinating question that merits further study. Sap-feeding instars are secondarily lost in Spinivalva (leaf miner of Passiflora ; Brito et al. 2013) and in several non-leaf-mining genera, including Epicephala .
The seed-feeding habit of Epicephala is unique within Gracillariidae. Nevertheless, deviations from the typical leaf-mining habit occur in a number of groups. Caloptilia species, which are common herbivores of Glochidion plants (Chap. 7), are sap-feeders as early instars, but later-instar larvae construct leaf roll s in which they live for the rest of the larval period. Larvae inside leaf rolls feed externally on the inner portions of folded leaves (Fig. 5.1). Galling has evolved in a number of gracillariid genera independently, for example, in Caloptilia (Kumata 1966; Fig. 5.1), Borboryctis (Kumata et al. 1988), and Parectopa (Wise 1962). Some species mine plant parts other than the leaf, such as stems or branches ( Marmara , Dendrorycter , Spulerina ) or fruit peel ( Marmara , Spulerina ). Others are plant-borers that use the seed ( Epicephala , Conopomorpha ), bud ( Stomphastis , Conopobathra , Chileoptilia ; Vargas and Landry 2005), or stem gall induced by rust fungi ( Polysoma ; Bashford 2002). Presumably, many more feeding types await discovery. Although the ultimate factor facilitating transitions from leaf mining to alternative feeding habits remains unknown, escape from parasitoid attack is probably a major reason for its evolution, as the structures they construct (leaf roll), induce (gall), or utilize (seed, bud, or fungal gall) are often protective against oviposition by parasitoids.
Gracillariidae species generally have narrow diet s, and each specializes upon one or a few species in a single plant genus or, less commonly, in multiple related genera. Exceptions include Acrocercops transecta , which feeds on Juglandaceae and Ericaceae (Ohshima 2008); Calybites phasianipennella , which uses Polygonaceae and Myrsinaceae (Kumata 1982); and several stem- or fruit-feeding species with exceptionally wide host ranges spanning multiple families ( Marmara , Conopomorpha ). Hosts of Gracillariidae are found in 93 diverse angiosperm families, although only three gracillariid species are known to feed on monocots: Acrocercops maranthaceae (Maranthaceae ; Busck 1934), Marmara smilacisella (Smilacaceae ; Braun 1909), and Gibbovalva tricuneatella (Typhaceae ; Sugisima et al. 2005). Parectopa leucocyma , the only known gymnosperm leaf-miner, feeds on Agathis australis in New Zealand (Wise 1962), and several undescribed gracillariid species are found on Podocarpus and Gnetum in Japan and Southeast Asia, respectively. No gracillariids are known to attack fern s or bryophyte s. For reasons presently unknown, Gracillariidae predominantly use woody hosts, a pattern also observed in certain other groups of leaf-miners (e.g., Nepticulidae , Heliozelidae ). The scarcity of monocot hosts may thus reflect the rarity of woody monocots rather than a true lack of preference.
Gracillariidae species have traditionally been classified into four subfamilies: Gracillariinae , Lithocolletinae , Phyllocnistinae , and Oecophyllembiinae (Kumata et al. 1988a,b; Kumata 1998; note that the circumscription of subfamilies varies among authors). Among these families, Gracillariinae contains by far the largest number of species (>1380), and it has been further divided by Kumata et al. (1988a,b) into four genus groups: Parornix-, Acrocercops-, Gracillaria-, and Parectopa-groups. Kawahara et al. (2017) recently provided a robust phylogenetic framework for the family based on the sequences of 22 genes, and proposed a new classification consisting of eight subfamilies: Acrocercopinae , Gracillariinae , Lithocolletinae , Marmarinae , Oecophyllembiinae , Ornixolinae , Parornichinae , and Phyllocnistinae (Table 5.1).
Epicephala belongs to the Ornixolinae subfamily (corresponding to the Parectopa group of Kumata et al. 1988a,b), which, unlike other subfamilies that have high species diversity in temperate zones, is concentrated in the tropics. Therefore, the numbers of genera and species are likely to increase dramatically with further taxonomic studies. Ornixolinae is also unique among Gracillariidae in that it contains a disproportionately high number of non-leaf-mining species. In fact, the plant borers listed above ( Epicephala , Conopomorpha , Stomphastis , Conopobathra , Chileoptilia , and Polysoma ) all belong to Ornixolinae. Thus, there may have been an evolutionary precursor within the Ornixolinae lineage that enabled repeated transitions from leaf-mining to boring feeding habits, giving rise to Epicephala.
2 Phylogeny of Epicephala
The genus Epicephala was described by Meyrick (1881) based on specimens collected in Sydney, Australia. Meyrick, the founder of modern Microlepidoptera systematics, made the greatest contribution to Epicephala taxonomy, eventually describing more than 20 Epicephala species from various parts of the Old World . However, several of the species described by Meyrick (e.g., Stomphastis chalybacma ) were transferred to other genera after detailed examination of genital morphology by later authors. A few more species currently placed in Epicephala will likely be subject to such taxonomic rearrangements. Concurrently with Meyrick, Turner greatly advanced the knowledge of Epicephala fauna in Australia , naming 11 currently accepted species. He was the first to note that Epicephala are seed-feeders; he observed Epicephala adults emerging from the capsules of Glochidion ferdinandii in Brisbane, Australia (Turner 1913). He named the moth E. frugicola , but later synonymized the species with E. colymbetella , the type species of the genus. Later, Vári (1961) described six Epicephala species from South Africa and provided the first detailed illustrations of the genitalia for Epicephala (as well as for many other genera of Gracillariidae). The study of Epicephala slowed down during the late twentieth century, during which time only three species were described (from Russia , Nigeria , and the Marquesas Islands ).
The taxonomy of Epicephala has attracted renewed interest since the discovery of obligate pollination mutualism (Kato et al. 2003). Li and colleagues, working on Epicephala found in China , described 20 species associated with Glochidion, Breynia, and Phyllanthus, and provided detailed descriptions of adult behavior and morphology for some of them. Kawakita and Kato (2016) reviewed the Japanese fauna of Epicephala and described seven species. As of April 2016, the genus contains 64 species (Table 5.2; Fig. 5.2). However, ecological, molecular, and biogeographical data suggest that the genus contains several hundred species (Kawakita 2010). For example, some clades of Epicephala are confined to Madagascar or New Caledonia , where none of the described Epicephala species occurs (Kawakita and Kato 2009). These regions are known for hotspots of Phyllanthus diversity, and thus potentially have large numbers of undescribed Epicephala species. There is also a high level of Phyllanthus diversity in the New World , where Epicephala has not been previously recorded; furthermore, as detailed in the following section, Epicephala is also prevalent in the Neotropics . Accelerating the taxonomy of Epicephala at a global scale is therefore critical for facilitating the ecological and evolutionary study of this model group.
Figure 5.3 shows the most recent analysis of the phylogenetic relationships among Epicephala (Kawakita and Kato 2016). Seven clades can be recognized, each of which is generally associated with a particular clade of Phyllantheae. An exception is Clade 2, which consists of species associated with herbaceous Phyllanthus belonging to various Phyllanthus subgenera. Conopomorpha flueggella , which is a nonpollinating seed-feeder of Flueggea suffruticosa , is depicted as a sister to Epicephala in Fig. 5.3. However, the phylogenetic position of C. flueggella is contentious because the species is sometimes placed as a sister to Clade 7 (Fig. 5.3). Conopomorpha flueggella clearly lacks pollination behavior, and lays eggs in buds or young fruits as well as flowers (Fig. 5.4). It also lacks an ovipositor , placing its eggs on the surface of the ovule (Fig. 5.4). Interestingly, ovipositing females sometimes take nectar with their proboscises prior to oviposition (Fig. 5.4) in a manner similar to Epicephala’s use of its proboscis to pollinate. The nectaring behavior of C. flueggella may have been the evolutionary precursor for active pollination; however, this question requires a robust understanding of the phylogenetic placement of C. flueggella with respect to Epicephala. At present, it is equally probable that the behavior of C. flueggella represents a secondary loss of pollination behavior. A hatched C. flueggella larva usually consumes all six seeds contained in each fruit of Flueggea suffruticosa (Fig. 5.4).
Conopomorpha flueggella was described by Hu et al. (2011), who placed it in the genus Conopomorpha based mainly on wing morphology. However, the true Conopomorpha , which include species that attack seeds of tropical fruit trees such as lychee and longan (Sapindaceae ) and cacao (Malvaceae ), are distantly related to Conopomorpha flueggella or Epicephala within Ornixolinae. Therefore, C. flueggella can likely be more accurately placed in a separate genus.
The basal-most Epicephala are the clade of moths associated with the Phyllanthus section Gomphidium in New Caledonia (Fig. 5.3). They clearly exhibit active pollination behavior (Chap. 3), but lack the sensilla on the proboscis and ovipositor that characterize the derived members of Epicephala. As such, they retain the morphology of the earliest Epicephala to acquire active pollination behavior. They lay eggs on the surface of the pistils (Fig. 5.5), and a single hatched larva consumes all the seeds contained in each fruit. However, moth mortality is very high, probably owing to desiccation during the egg stage. This high mortality is necessary for a fraction of the seeds to remain intact despite destructive seed-feeding by the larvae (Chap. 3). Because there is a large morphological disparity between moths of this clade and those of the derived Epicephala, especially with respect to the female genitalia, the former should probably be placed in a separate genus. However, determining whether it is congeneric with C. flueggella requires a closer examination of morphology and a better resolution of the basal phylogenetic relationships.
The remaining moths can safely be placed in Epicephala, and share the female ovipositor as a morphological synapomorphy (Clades 1–6; Figs. 5.3, 5.5). Ovipositors are not known in any other Gracillariidae genus; thus, aside from pollination behavior, they represent the trait that best characterizes Epicephala. The development of the ovipositor is most likely an adaptation for laying eggs internally in floral tissue, thereby avoiding egg desiccation (Fig. 5.5).
Interestingly, there is considerable variation in egg placement behavior among Epicephala species. Most Epicephala species associated with Glochidion lay eggs either through the apical pit of the stylar column into the stylar tissue or laterally through the ovary wall on the surface of the ovule (Fig. 5.6). This difference in oviposition mode is reflected in morphology; the ovipositor s of laterally ovipositing species are distinctly more angular than those of apically ovipositing species (Kawakita and Kato 2016; Fig. 5.6).
Certain species associated with Phyllanthus and Glochidion lay eggs in the pedicels of female flowers (Chap. 10). In such species, the hatched larvae initially bore through the pedicel to enter the ovary. Epicephala vitisidaea and E. mirivalvata lay eggs in the narrow space between the sepals and ovary of their host Breynia plants, having thus reverted to external oviposition (Kawakita and Kato 2004; Zhang et al. 2012a), although both species have retained functional ovipositors. Because Phyllantheae plants are known to abort selectively those flowers with heavy egg loads and abortion is likely based on the extent of mechanical damage to flowers (Chap. 9), external oviposition in these species may have evolved to circumvent the abortion response in their host plants.
However, the adaptive significance of other oviposition modes is less clear. In cases where two or more Epicephala species co-occur on the same Phyllantheae host, the different species exhibit different oviposition behaviors (Kawakita et al. 2015; Kawakita and Kato 2016). This may indicate that different oviposition strategies are necessary for stable coexistence on shared hosts.
Another distinguishing characteristic of the core Epicephala clade is the numerous sensilla on the proboscis es of females (Fig. 5.7). Sensilla are absent in males, and a sensilla-bearing proboscis is not known in any other genera of Gracillariidae. Thus, we can infer that the function of the sensilla is linked to active pollination. Because most pollen is held on the basal area of the proboscis of pollen-carrying females where the density of sensilla is highest, females are able to carry more pollen than would be possible in the absence of such a structure (Fig. 5.7). Support for the interpretation that the sensilla assist in pollination comes from the absence of sensilla in species that have secondarily lost the pollination behavior. For example, of the six major lineages of the core Epicephala clade, the herbaceous Phyllanthus clade consists of species that lay eggs in young fruits of herbaceous Phyllanthus and thus do not pollinate flowers. Accordingly, the sensilla on their proboscises are lost entirely or are rudimentary (Fig. 5.7). The Phyllanthus reticulatus clade represents another Epicephala lineage that lost the sensilla. Of the six species associated with plants of the Phyllanthus reticulatus species complex in Taiwan, three induce gall formation on female flowers, although two of them retain pollination behavior. Sensilla are completely lost in the three gall-inducing species, probably because selection to transfer pollen is relaxed or absent owing to their ability to induce galls (Chap. 11).
As mentioned in the previous section, gall-inducers have arisen repeatedly in the course of gracillariid evolution, but the evolution of galling may be particularly common in Epicephala. In the Ryukyu Archipelago of southern Japan, E. corruptrix is associated with two Glochidion species ( G. obovatum and G. rubrum ). On both hosts, E. corruptrix exhibits pollination behavior, but the resulting fruits do not develop normally. Instead, the locule in which the larva develops grows irregularly and eventually becomes a gall (Fig. 5.8). Populations of G. obovatum and G. rubrum associated with E. corruptrix suffer very low seed production. This contrasts sharply with populations elsewhere in their ranges, where the plants are pollinated by non-gall-inducing E. obovatella , and produce large numbers of normal fruits and seeds. Epicephala corruptrix is distantly related to the gall-inducers of the Phyllanthus reticulatus species complex, so the galling habit has independently evolved at least twice in Epicephala. Similar gall-like development is found in P. humbertii in Madagascar and P. cuscutiflorus in Australia. It is therefore interesting to consider how many other lineages of Epicephala evolved the gall-inducing ability. The adaptive significance of galling is still unclear, but is probably linked to escape from parasitoid attack (Chap. 11).
3 Global Diversity of Epicephala
The genus Epicephala has thus far been described only in the Old World tropics , but they are also prevalent in the Neotropics . Observation of Phyllanthus in Cuba and Jamaica indicate that several species in the subgenus Xylophylla are associated with seed-feeding Epicephala. Some of the these Phyllanthus species (e.g., P. chamaecrystoides , P. myrtilloides ) bear female flowers with fused styles characteristic of Epicephala-pollinated plants in the Old World, whereas others possess bifid and spread styles indicative of pollination by nonspecialized insects (e.g., P. angustifolius , P. nutans ). Whether obligate pollination mutualism occurs in Xylophylla is still unclear, but the outcome of association between Xylophylla and Epicephala appears to be highly variable among species. There are roughly 60 species of Xylophylla, with the highest concentration of species being in the Caribbean islands, although the subgenus occurs as far south as Andean Peru.
The widespread occurrence of Epicephala in the New World is further demonstrated by the presence of Epicephala larvae and pupae on herbarium specimens (Fig. 5.9). Because plant specimens bearing fruits may sometimes contain Epicephala larvae at the time of collection, the larvae are occasionally found on Phyllanthus specimens, especially those in which the capsules dehisced while being dried. The larvae of most Epicephala species have a characteristic red color with narrow white bands, and cannot be mistaken for those of other Lepidoptera. Mature larvae inside fruits may also spin cocoon s on the edges of leaves before they are completely dried. While spinning cocoons, the larvae of Epicephala excrete bubblelike balls from the anus, grab them with the mandibles, and attach them to the surface of the cocoon through a hole punched from inside the cocoon (Fig. 5.9). Although the adaptive role of ball production is unknown, such a habit is known only in Epicephala and several related genera of the Ornixolinae . Therefore, the presence of such cocoons on herbarium specimens provides reliable evidence of an association with Epicephala.
Epicephala larvae and cocoons are often found on specimens of Phyllanthus section Nothoclema (subgenus Conami; Fig. 5.9; Table 5.3). The group contains 10 species distributed from Mexico to Argentina, and is often a prominent component of the local flora. The female flowers of the Nothoclema species have spread styles and do not appear to be specialized to Epicephala; thus, it would be interesting to clarify the pollination system of Nothoclema plants to understand whether obligate pollination mutualism occurs in the New World. One surprising finding was an association between Epicephala and Flueggea elliptica (Table 5.3), a plant that is only known from a small coastal area in southernmost Ecuador . The Old World Flueggea suffruticosa is host to Conopomorpha flueggella and Epicephala relictella , but other Flueggea species, such as the widespread and abundant F. virosa , have never been found hosting Epicephala. The Flueggea–Epicephala association in the New World is probably phylogenetically independent from that found in Asia, but determining where the Ecuadorian species belong within the Epicephala phylogeny is critical for the global understanding of Epicephala diversity and evolution.
Finally, one exciting possibility is the occurrence of obligate pollination mutualism on the tepuis of the Guiana Highlands . The tepui s are table-top mountains of granite arenite sandstone rising abruptly from the Amazonian rainforest that are host to a spectacular array of endemic plants and animals. The majority of the tepuis occur in Venezuela and Western Guyana , but some are also found in Colombia , Suriname , French Guiana , and in northernmost Brazil .
The Phyllanthus species found in the Guiana Highlands are grouped into a well-defined section, Microglochidion (Webster and Carpenter 2002, 2008). Many species possess elongated, nonbifid, and fused styles, which strikingly resemble those of Glochidion or New Caledonian Phyllanthus. Although neither larvae nor cocoons of Epicephala were found on herbarium specimens, the seeds of several Microglochidion species have holes that are typical of those made by Epicephala larvae, suggesting that the association with Epicephala is widespread among the ~10 species of Guiana Highland Phyllanthus (Table 5.3). It is exciting to think of the possibility that obligate pollination mutualism, which probably originated in the Old World, has reached some of the most exotic biota on earth and produced an impressive number of endemic species.
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Kawakita, A., Kato, M. (2017). Diversity of Pollinator Moths. In: Kato, M., Kawakita, A. (eds) Obligate Pollination Mutualism. Ecological Research Monographs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56532-1_5
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