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Plant-insect interactions from Middle Triassic (late Ladinian) of Monte Agnello (Dolomites, N-Italy)-initial pattern and response to abiotic environmental perturbations.

Wappler T, Kustatscher E, Dellantonio E - PeerJ (2015)

Bottom Line: The flora from Monte Agnello is distinctive, due to its preservation in subaerially deposited pyroclastic layers with exceptionally preserved details.Thus, the para-autochthonous assemblage provides insights into environmental disturbances, caused by volcanic activity, and how they profoundly affected the structure and composition of herbivory patterns.These DT patterns show that external foliage feeders, piercer-and-suckers, leaf miners, gallers, and oviposition culprits were intricately using almost all tissue types from the dominant host plants of voltzialean conifers (e.g., Voltzia), horsetails, ferns (e.g., Neuropteridium, Phlebopteris, Cladophlebis and Thaumatopteris), seed ferns (e.g., Scytophyllum), and cycadophytes (e.g., Bjuvia and Nilssonia).

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Affiliation: Steinmann Institute, University of Bonn , Bonn , Germany.

ABSTRACT
The Paleozoic-Mesozoic transition is characterized by the most massive extinction of the Phanerozoic. Nevertheless, an impressive adaptive radiation of herbivorous insects occurred on gymnosperm-dominated floras not earlier than during the Middle to Late Triassic, penecontemporaneous with similar events worldwide, all which exhibit parallel expansions of generalized and mostly specialized insect herbivory on plants, expressed as insect damage on a various plant organs and tissues. The flora from Monte Agnello is distinctive, due to its preservation in subaerially deposited pyroclastic layers with exceptionally preserved details. Thus, the para-autochthonous assemblage provides insights into environmental disturbances, caused by volcanic activity, and how they profoundly affected the structure and composition of herbivory patterns. These diverse Middle Triassic biota supply extensive evidence for insect herbivore colonization, resulting in specific and complex herbivory patterns involving the frequency and diversity of 20 distinctive damage types (DTs). These DT patterns show that external foliage feeders, piercer-and-suckers, leaf miners, gallers, and oviposition culprits were intricately using almost all tissue types from the dominant host plants of voltzialean conifers (e.g., Voltzia), horsetails, ferns (e.g., Neuropteridium, Phlebopteris, Cladophlebis and Thaumatopteris), seed ferns (e.g., Scytophyllum), and cycadophytes (e.g., Bjuvia and Nilssonia).

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Related in: MedlinePlus

Examples of internal foliage consumption at Monte Agnello (Dolomites, N-Italy).(A)–(B) Elliptical piercing and sucking punctures on the conifer Voltzia sp. 1 (MGP196/35), enlarged in (B) (DT48). (C) Ellipsoidal, sessile bud gall from branchlet (DT121) on the unaffiliated Voltzia sp. 1 (MGP171/81). (D) Small, hemispherical, thoroughly carbonized structures (DT80) on Phlebopteris fiemmensisKustatscher et al., 2014 (MGP181/57C), indicated by arrows. (E) Fern Speirocarpus sp. (MGP197/69B) showing lenticular-ovoidal foliar oviopsition scars (DT101), indicated by arrows. (F) and (I) Lenticular-ovoidal foliar oviopsition scars (DT100) on the unaffiliated cycadophytes (MGP196/6; MGP196/7A). (G) Undifferentiated galling structures (DT80) on a seed-fern (MGP63/94), indicated by arrows. (H) Semilinear, frass-laden, mining structure with a smooth and rimmed margin (DT40) on Scytophyllum bergeriBornemann, 1856 (MGP63/98A), asterisk indicates initial place of oviposition. (J) Ellipsoidal scale impressions with roughened surface (DT128) on the cycadophyte Nilssonia cf. neuberi Stur ex Pott, Kerp & Krings, 2007 (DT128) (MGP194/72A). Scale bars: striped, 10 mm; solid, 5 mm; dotted, 1 mm.
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fig-3: Examples of internal foliage consumption at Monte Agnello (Dolomites, N-Italy).(A)–(B) Elliptical piercing and sucking punctures on the conifer Voltzia sp. 1 (MGP196/35), enlarged in (B) (DT48). (C) Ellipsoidal, sessile bud gall from branchlet (DT121) on the unaffiliated Voltzia sp. 1 (MGP171/81). (D) Small, hemispherical, thoroughly carbonized structures (DT80) on Phlebopteris fiemmensisKustatscher et al., 2014 (MGP181/57C), indicated by arrows. (E) Fern Speirocarpus sp. (MGP197/69B) showing lenticular-ovoidal foliar oviopsition scars (DT101), indicated by arrows. (F) and (I) Lenticular-ovoidal foliar oviopsition scars (DT100) on the unaffiliated cycadophytes (MGP196/6; MGP196/7A). (G) Undifferentiated galling structures (DT80) on a seed-fern (MGP63/94), indicated by arrows. (H) Semilinear, frass-laden, mining structure with a smooth and rimmed margin (DT40) on Scytophyllum bergeriBornemann, 1856 (MGP63/98A), asterisk indicates initial place of oviposition. (J) Ellipsoidal scale impressions with roughened surface (DT128) on the cycadophyte Nilssonia cf. neuberi Stur ex Pott, Kerp & Krings, 2007 (DT128) (MGP194/72A). Scale bars: striped, 10 mm; solid, 5 mm; dotted, 1 mm.

Mentions: Of the 684 plant remains examined from the Monte Agnello flora, 83, or 12.13%, exhibit some sort of damage represented by 20 different damage types. The taxa or morphotypes examined were represented by foliage, axes, stem fragments, fructifications, and dispersed seeds (Table 2). A total of 95 damage type occurrences were observed throughout the bulk flora: 45 on cycadophytes (representing 36.5% of all specimens), 37 on seed ferns (8.0%), ten on conifers (44.3%), and three on ferns (7.6%) (Table 3), suggesting that selective feeding by insect herbivores preferentially targeted particular seed plants. This pattern of selectivity was also recognized within the early late Permian (Wuchiapingian) of the Gröden/Val Gardena Sandstone from the Bletterbach Gorge of the Dolomites (Northern Italy) (T Wappler, pers. obs., 2013). Herbivory recorded for the Monte Agnello sites represents nearly all of the fundamental modes of herbivory, excluding fungal infection, which was not observed (see Gunkel & Wappler, 2015). Multiple DTs or functional feeding groups were only recorded in 1.6% of the plant remains whereas the majority were only damaged in one way (∼11%). Seven distinctive functional feeding groups have been detected on the foliar elements from Monte Agnello, most of which occur on particular plant hosts. Types of the external foliage feeding constitute 78.9% of all DT occurrences and preferentially occurred on the seed fern S. bergeri and consists of the exophytic consumption of live plant tissues, subdivided into skeletonization and margin-, hole- and surface feeding; this is the most common ensemble of Triassic damage types (Labandeira & Prevec, 2014; T Wappler, pers. obs., 2013) (Fig. 2). Those of the galling FFG provided 11.5% of all DT occurrences and are more or less evenly distributed among conifers, ferns and seed ferns (Figs. 3C–3D and 3G). Galling represents the most biologically complex of all major interactions, and represents arthropod-induced abnormal cell proliferation that can occur on all major plant organs (e.g., Kustatscher et al., 2014; Scott, Anderson & Anderson, 2004); examples are widely known (e.g., Stone & Schönrogge, 2003). Oviposition, though not a feeding interaction, comprised 5.2% of all DT occurrences; examples are common (Ghosh, Kar & Chatterjee, 2015; McLoughlin, 2011) (Figs. 3E–3F and 1). Minor levels of insect damage were present for piercing-and-sucking (2.1% of all DT occurrences; Fig. 3J) and mining (1.1%; Fig. 3H) FFGs. Leafminers construct distinct leaf mines, most of which are quite conspicuous and represent a form of endophagous herbivory in which a herbivore targets and feeds on fluid tissues such as phloem, mesophyll or epidermal cell protoplasts (Sinclair & Hughes, 2010); examples are uncommon and the possible mining structure on the pteridosperm Scytophyllum bergeri (Fig. 3H) indicates that the origin and diversification of the leaf-mining habit occurred about 92 million years before the first appearance of fossil angiosperms (Ash, 1997; Gnaedinger, Adami-Rodrigues & Gallego, 2014; Kustatscher et al., 2014; McLoughlin, 2011; Moisan et al., 2012; Pott et al., 2008).


Plant-insect interactions from Middle Triassic (late Ladinian) of Monte Agnello (Dolomites, N-Italy)-initial pattern and response to abiotic environmental perturbations.

Wappler T, Kustatscher E, Dellantonio E - PeerJ (2015)

Examples of internal foliage consumption at Monte Agnello (Dolomites, N-Italy).(A)–(B) Elliptical piercing and sucking punctures on the conifer Voltzia sp. 1 (MGP196/35), enlarged in (B) (DT48). (C) Ellipsoidal, sessile bud gall from branchlet (DT121) on the unaffiliated Voltzia sp. 1 (MGP171/81). (D) Small, hemispherical, thoroughly carbonized structures (DT80) on Phlebopteris fiemmensisKustatscher et al., 2014 (MGP181/57C), indicated by arrows. (E) Fern Speirocarpus sp. (MGP197/69B) showing lenticular-ovoidal foliar oviopsition scars (DT101), indicated by arrows. (F) and (I) Lenticular-ovoidal foliar oviopsition scars (DT100) on the unaffiliated cycadophytes (MGP196/6; MGP196/7A). (G) Undifferentiated galling structures (DT80) on a seed-fern (MGP63/94), indicated by arrows. (H) Semilinear, frass-laden, mining structure with a smooth and rimmed margin (DT40) on Scytophyllum bergeriBornemann, 1856 (MGP63/98A), asterisk indicates initial place of oviposition. (J) Ellipsoidal scale impressions with roughened surface (DT128) on the cycadophyte Nilssonia cf. neuberi Stur ex Pott, Kerp & Krings, 2007 (DT128) (MGP194/72A). Scale bars: striped, 10 mm; solid, 5 mm; dotted, 1 mm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4419555&req=5

fig-3: Examples of internal foliage consumption at Monte Agnello (Dolomites, N-Italy).(A)–(B) Elliptical piercing and sucking punctures on the conifer Voltzia sp. 1 (MGP196/35), enlarged in (B) (DT48). (C) Ellipsoidal, sessile bud gall from branchlet (DT121) on the unaffiliated Voltzia sp. 1 (MGP171/81). (D) Small, hemispherical, thoroughly carbonized structures (DT80) on Phlebopteris fiemmensisKustatscher et al., 2014 (MGP181/57C), indicated by arrows. (E) Fern Speirocarpus sp. (MGP197/69B) showing lenticular-ovoidal foliar oviopsition scars (DT101), indicated by arrows. (F) and (I) Lenticular-ovoidal foliar oviopsition scars (DT100) on the unaffiliated cycadophytes (MGP196/6; MGP196/7A). (G) Undifferentiated galling structures (DT80) on a seed-fern (MGP63/94), indicated by arrows. (H) Semilinear, frass-laden, mining structure with a smooth and rimmed margin (DT40) on Scytophyllum bergeriBornemann, 1856 (MGP63/98A), asterisk indicates initial place of oviposition. (J) Ellipsoidal scale impressions with roughened surface (DT128) on the cycadophyte Nilssonia cf. neuberi Stur ex Pott, Kerp & Krings, 2007 (DT128) (MGP194/72A). Scale bars: striped, 10 mm; solid, 5 mm; dotted, 1 mm.
Mentions: Of the 684 plant remains examined from the Monte Agnello flora, 83, or 12.13%, exhibit some sort of damage represented by 20 different damage types. The taxa or morphotypes examined were represented by foliage, axes, stem fragments, fructifications, and dispersed seeds (Table 2). A total of 95 damage type occurrences were observed throughout the bulk flora: 45 on cycadophytes (representing 36.5% of all specimens), 37 on seed ferns (8.0%), ten on conifers (44.3%), and three on ferns (7.6%) (Table 3), suggesting that selective feeding by insect herbivores preferentially targeted particular seed plants. This pattern of selectivity was also recognized within the early late Permian (Wuchiapingian) of the Gröden/Val Gardena Sandstone from the Bletterbach Gorge of the Dolomites (Northern Italy) (T Wappler, pers. obs., 2013). Herbivory recorded for the Monte Agnello sites represents nearly all of the fundamental modes of herbivory, excluding fungal infection, which was not observed (see Gunkel & Wappler, 2015). Multiple DTs or functional feeding groups were only recorded in 1.6% of the plant remains whereas the majority were only damaged in one way (∼11%). Seven distinctive functional feeding groups have been detected on the foliar elements from Monte Agnello, most of which occur on particular plant hosts. Types of the external foliage feeding constitute 78.9% of all DT occurrences and preferentially occurred on the seed fern S. bergeri and consists of the exophytic consumption of live plant tissues, subdivided into skeletonization and margin-, hole- and surface feeding; this is the most common ensemble of Triassic damage types (Labandeira & Prevec, 2014; T Wappler, pers. obs., 2013) (Fig. 2). Those of the galling FFG provided 11.5% of all DT occurrences and are more or less evenly distributed among conifers, ferns and seed ferns (Figs. 3C–3D and 3G). Galling represents the most biologically complex of all major interactions, and represents arthropod-induced abnormal cell proliferation that can occur on all major plant organs (e.g., Kustatscher et al., 2014; Scott, Anderson & Anderson, 2004); examples are widely known (e.g., Stone & Schönrogge, 2003). Oviposition, though not a feeding interaction, comprised 5.2% of all DT occurrences; examples are common (Ghosh, Kar & Chatterjee, 2015; McLoughlin, 2011) (Figs. 3E–3F and 1). Minor levels of insect damage were present for piercing-and-sucking (2.1% of all DT occurrences; Fig. 3J) and mining (1.1%; Fig. 3H) FFGs. Leafminers construct distinct leaf mines, most of which are quite conspicuous and represent a form of endophagous herbivory in which a herbivore targets and feeds on fluid tissues such as phloem, mesophyll or epidermal cell protoplasts (Sinclair & Hughes, 2010); examples are uncommon and the possible mining structure on the pteridosperm Scytophyllum bergeri (Fig. 3H) indicates that the origin and diversification of the leaf-mining habit occurred about 92 million years before the first appearance of fossil angiosperms (Ash, 1997; Gnaedinger, Adami-Rodrigues & Gallego, 2014; Kustatscher et al., 2014; McLoughlin, 2011; Moisan et al., 2012; Pott et al., 2008).

Bottom Line: The flora from Monte Agnello is distinctive, due to its preservation in subaerially deposited pyroclastic layers with exceptionally preserved details.Thus, the para-autochthonous assemblage provides insights into environmental disturbances, caused by volcanic activity, and how they profoundly affected the structure and composition of herbivory patterns.These DT patterns show that external foliage feeders, piercer-and-suckers, leaf miners, gallers, and oviposition culprits were intricately using almost all tissue types from the dominant host plants of voltzialean conifers (e.g., Voltzia), horsetails, ferns (e.g., Neuropteridium, Phlebopteris, Cladophlebis and Thaumatopteris), seed ferns (e.g., Scytophyllum), and cycadophytes (e.g., Bjuvia and Nilssonia).

View Article: PubMed Central - HTML - PubMed

Affiliation: Steinmann Institute, University of Bonn , Bonn , Germany.

ABSTRACT
The Paleozoic-Mesozoic transition is characterized by the most massive extinction of the Phanerozoic. Nevertheless, an impressive adaptive radiation of herbivorous insects occurred on gymnosperm-dominated floras not earlier than during the Middle to Late Triassic, penecontemporaneous with similar events worldwide, all which exhibit parallel expansions of generalized and mostly specialized insect herbivory on plants, expressed as insect damage on a various plant organs and tissues. The flora from Monte Agnello is distinctive, due to its preservation in subaerially deposited pyroclastic layers with exceptionally preserved details. Thus, the para-autochthonous assemblage provides insights into environmental disturbances, caused by volcanic activity, and how they profoundly affected the structure and composition of herbivory patterns. These diverse Middle Triassic biota supply extensive evidence for insect herbivore colonization, resulting in specific and complex herbivory patterns involving the frequency and diversity of 20 distinctive damage types (DTs). These DT patterns show that external foliage feeders, piercer-and-suckers, leaf miners, gallers, and oviposition culprits were intricately using almost all tissue types from the dominant host plants of voltzialean conifers (e.g., Voltzia), horsetails, ferns (e.g., Neuropteridium, Phlebopteris, Cladophlebis and Thaumatopteris), seed ferns (e.g., Scytophyllum), and cycadophytes (e.g., Bjuvia and Nilssonia).

No MeSH data available.


Related in: MedlinePlus