Herbivory in early Tertiary Arctic forests

Palaeogeography, Palaeoclimatology, Palaeoecology 310 (2011) 283–295

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Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o

Herbivory in early Tertiary Arctic forests Torsten Wappler a,⁎, Thomas Denk b a b

Steinmann Institute for Geology, Mineralogy and Palaeontology, Division Palaeontology, University of Bonn, Nussallee 8, D-53115 Bonn, Germany Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden

a r t i c l e

i n f o

Article history: Received 24 March 2011 Received in revised form 8 July 2011 Accepted 16 July 2011 Available online 23 July 2011 Keywords: Palaeogene Herbivory Plant–insect interactions Arctic fossil forests Latitudinal gradient Spitsbergen

a b s t r a c t Early Tertiary High Arctic forest ecosystems are unique in that they have no equivalent among modern forests. Today, no forest ecosystem exists at such high latitudes. To assess the potential role of herbivory during the early Tertiary warm period at high latitudes, we have surveyed 1567 fossil angiosperm leaves from Svalbard for the presence or absence of 35 insect damage types (DTs). Our investigation for the first time uncovered a wealth of insect trace fossils from the early Tertiary northern high latitudes. These include galls, mines, and feeding traces on fossil leaves. Most of the folivory includes unspecific external foliage feeding that cannot be ascribed to a particular group of insects. Exceptions are the mining damage types that are most similar to those made by leaf-mining moths (Lepidoptera: Gracillaroidea). Nevertheless, the abundance of folivory indicates that herbivorous insects were an important component of the forests thriving in the Arctic realm. The observed change in insect herbivory from the Middle Paleocene to the Late Eocene/Early Oligocene in Spitsbergen may be attributed to climatic variables because they influence insect life-cycle timing, population density, and geographic range. © 2011 Elsevier B.V. All rights reserved.

1. Introduction The Arctic is one of the most fragile ecosystems on Earth; it is also under immense environmental pressure as the effects of current global warming are felt most acutely at northern latitudes (e.g. Hodkinson et al., 1998; Jónsdóttir, 2005; Budikova, 2009; Fiorillo and McCarthy, 2010). Today, the vegetation is characterized by tundra ecosystems and polar semidesert communities. To the extreme north is the polar desert, where only about 5% of the ground surface is covered by herb– cryptogam communities. In stark contrast, during the Palaeogene, broadleaved deciduous forests were able to grow at northern high latitudes (e.g. Schweitzer, 1974,1980; Greenwood and Basinger, 1994; McIver and Basinger, 1999; Abbott and Brochmann, 2003; Jahren, 2007; Jahren and Sternberg, 2008; Budantsev and Golovneva, 2010). The Arctic fossil ecosystem consisiting of rich broadleaved deciduous and coniferous forests was markedly different from ecosystems presently occuring in the High Arctic. Early Tertiary (Paleocene–Eocene/Oligocene) floras from Spitsbergen (Svalbard) rank among the best documented within the Arctic region from studies of leaves. At the Swedish Museum of Natural History, about ~4500 specimens of leaf fossils from the early Tertiary of Spitsbergen are deposited. Given the high palaeolatitude and absence of large polar ice caps, the fossil assemblage from Spitsbergen is unique in Europe. Insect body fossils are rare in Paleocene to Early Oligocene

⁎ Corresponding author. Tel.: + 49228734682; fax: + 49228733509. E-mail address: [email protected] (T. Wappler). 0031-0182/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2011.07.020

sedimentary rocks from Spitsbergen (Birket-Smith, 1977). Despite this, the rich record of fossil leaves along with the type of sediments preserving these fossils makes it possible to study herbivorous insects using their specific feeding traces. Studies of the Tertiary floras of Spitsbergen (e.g. Kvaček et al., 1994; Birkenmajer and Zastawniak, 2005; Uhl et al., 2007; Budantsev and Golovneva, 2010 and references herein) have focused primarily on the systematic affinity of the flora, or the use of fossil leaves to estimate palaeoclimate (Golovneva, 2000; Uhl et al., 2007; Eldrett et al., 2009; Greenwood et al., 2010). In contrast, plant/insect associations and their role for interpreting palaeoenvironmental signals of ancient Arctic ecosystems, particularly in the Northern Hemisphere, have rarely been studied (but see Sunderlin et al., 2011). Regional floras appear to have undergone significant re-organization during the Palaeogene, involving migration, evolution of new taxa, and extinction at least in middle latitudes (e.g. Greenwood and Basinger, 1994; Askin and Spicer, 1995; Harrington and Jaramillo, 2007). Uncertainties remain, however, over the response of vegetation to long-term climate change at high latitudes, and the shift in the character of the vegetation from the Paleocene to the Eocene, as well as from the ‘hothouse world’ of the early Palaeogene to the ‘icehouse world’ of the Oligocene (e.g. Schouten et al., 2008). For the Palaeogene, it has been noted that at lower latitudes of the Northern Hemisphere herbivory increased as the vegetation changed from temperate to subtropical (e.g. Wilf and Labandeira, 1999; Currano et al., 2008,2010). This temporal trend is comparable to the present geographical gradient from the mid latitudes to the tropics (Greenwood and Wing, 1995; Wilf et al., 2001; Wing et al., 2009). Terrestrial biodiversity and temporal trends in the

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diversity of interactions, including plant–herbivore trophic links at high latitudes are less well understood (e.g. Ollerton and Cranmer, 2002; Netherer and Schopf, 2010). A primary goal of the present study is to use evidence from plant/ insect associations at different fossil localities in Spitsbergen to (1) assess how plant and insects associated and evolved in these environments, and (2) how plant–insect associations at high latitudes differ from contemporaneous European mid-latitude associations (Wappler et al., 2009). Furthermore, changing patterns of herbivory during the early Tertiary in the Arctic are described within a palaeoclimatic framework. 2. Tertiary rocks of Spitsbergen 2.1. Geological setting and palaeoecology Spitsbergen is located in the northwestern corner of the Barents Shelf at 74–81°N and 10–30°E (Fig. 1). The archipelago represents an uplifted part of this otherwise submerged shelf. The uplift was most extensive in the north and west, leaving progressively older rocks in these directions. A pronounced synclinal feature, the Tertiary Central Spitsbergen Basin, occupies most of central Spitsbergen. The basin is bounded to the west by the West Spitsbergen fold- and thrust-belt, which wedges out towards the eastern part of Spitsbergen (e.g. Dallmann et al., 1993; Birkenmajer, 2006). The Tertiary Central

Spitsbergen Basin may be regarded as a regional foreland depression with cyclic infill of mixed continental to marine clastics. These form an overall transgressive package, from coal-bearing deltaic deposits to marine sandstones and shales, characterising the transtensional phase (Helland-Hansen, 1990; Dallmann et al., 1999). Most of the plant fossils in the Central Tertiary Basins are found in the Firkanten and Aspelintoppen Formations (part of the Van Mijenfjorden Group sensu Harland, 1969), as well as in the Renardodden area, part of the Calypsostranda Group (according to Dallmann et al., 1999) (see also supplementary material in Appendix A). 2.1.1. Firkanten Formation The Firkanten Formation is part of the Van Mijenfjorden Group; it is 100 to 170 m thick. The lower part is coal-bearing, comprising the most important coal deposits of Spitsbergen. Alternating with the coal are marine and non-marine sandstones, siltstones, and shales. While the lower part of the Firkanten Fm. is deltaic in origin, the upper part is predominantly marine representing a series of barrier shoreline developments. An overall transgressive trend is characteristic of this unit (Dallmann et al., 1999). Schweitzer (1974, 1980) suggested that the flora of the Firkanten Fm. is derived from coastal bogs consisting of marshes with large open lakes, swamp forests of Taxodium, and mixed conifer and broadleaved deciduous forests. Denk et al. (1999) noted that the flora of the Firkanten Fm. is chiefly characterized by its rich conifer flora. Angiosperms are

Fig. 1. Generalized geological map of Spitsbergen, showing the area of Tertiary deposits in the Central Basin. Thick lines denote major fault systems. Numbers 1 to 3 refer to the stratigraphic level on the plant bearing localities. 1 — Firkanten Formation; 2 — Aspelintoppen Formation; 3 — Renardodden Flora (redrawn from Denk et al., 1999). Details for individual plant bearing localties see also supplementary material in Appendix A, Table S1.

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represented by plane trees and Trochodendroides (see also Budantsev and Golovneva, 2010). 2.1.2. Aspelintoppen Formation The Aspelintoppen Formation (Van Mijenfjorden Group) is over 1000 m thick and consists of sandstones with siltstones, mudstones, and thin coals. The deposits are distinctly terrestrial and represent shallow water deposits, such as distributary channels, crevasse splays, and swamp deposits (Dallmann et al., 1999). According to Schweitzer (1974), at the time of deposition of the Aspelintoppen Fm. tectonic uplift had isolated the Central Basin and extensive forests alternated with large inland lakes. Typical elements of lowland wetland areas (Glyptostrobus, Taxodium) were rare or missing. Denk et al. (1999) noted that the flora of the Aspelintoppen Fm. is markedly more diverse in angiosperm taxa, including modern types, such as Acer, Aesculus, and Ulmus (see also Budantsev and Golovneva, 2010). Among conifers, the high abundance of Metasequoia is characteristic. This appears to reflect a more varied landscape, involving wetlands, well-drained lowland forests, and upland forests. 2.1.3. Renardodden Flora The plant bearing sediments in the Renardodden area at the west mouth of Recherchefjorden belong to the Calypsostranda Group. The Calypsostranda Group is part of the West Spitsbergen fold- and thrustbelt and comprises two formations, the Skilvika Formation and the overlying Renardodden Formation, both of which are exposed between Skilvika to the northwest, Renardodden to the north, and Calypsobyen to the south (Dallmann et al., 1999). The plant bearing sediments of the Renardodden Flora are mainly belonging to the Skilvika Formation (Schweitzer, 1974; Birkenmajer, 2006). The strata are intercalated sandstones and siltstones with thin layers of bituminous shales and coal seams. They are cumulatively 335 m thick (Dallmann, 1989). According to Thiedig et al. (1979), the sediments are limnofluvial deposits in a small marginal basin and hence an origin similar to the sediments of the Aspelintoppen Formation is likely (Denk et al., 1999). 2.2. Age of the Tertiary sediments of Spitsbergen Precise ages of Tertiary sedimentary rock formations on Spitsbergen are still not entirely settled (Dallmann et al., 1993, 1999). Heer (1866, 1868–1883) suggested a Miocene age for all the formations based mainly on plant fossil evidence. Later, Vonderbank (1970) and Schweitzer (1974), based on plant and animal fossils, suggested that the lowermost Firkanten Formation should be dated as Paleocene. Older biostratigraphic work also assigned a Paleocene age to the Firkanten Formation (Ravn, 1922; Manum, 1962; Livšic, 1974). Dallmann et al. (1999), although assigning a conservative Paleocene age to the Firkanten Formation, consider the overlying Basilika Formation to be of Late Paleocene age. This would suggest an (later) Early to Middle Paleocene age for the Firkanten Formation. More recent data suggest that most of this formation was deposited after the Early Paleocene (e.g. Cepek, 2001). The younger formations of the Calypsostranda and Van Mijenfjorden Group (Renardodden Flora and Aspelintoppen Fm.) are generally accepted to be pre-Oligocene in age, but unambiguous biostratigraphic information for the Renardodden Flora and the Aspelintoppen Formation is not available. Dallmann et al. (1999) accept a Late Eocene to Early Oligocene age for the Calypsostrands Group (Renardodden Flora), but consider the age of the Aspelintoppen Fm. to be unsettled (“?Eocene–?Oligocene”). Crabaugh and Steel (2004) tentatively placed the Lower to Middle Eocene transition in the middle part of the Aspelintoppen Formation, while dinocysts indicate an unresolved Eocene age (Manum and Throndsen, 1986). Generally, microfossils are badly preserved and it is therefore difficult to obtain conclusive results. For the present account we followed Dallmann et al. (1999). Thus, the Firkanten Formation would be (late) Early to Middle Paleocene in age, whereas the Renardodden Flora would be Late Eocene

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(to Early Oligocene) in age. The Aspelintoppen Formation is younger than the Firkanten Formation but its age is uncertain relative to the Renardodden Flora (see also Fig. S1). 3. Material and methods This study is based on the extensive collection of Palaeogene fossil leaves from Spitsbergen, housed at the Naturhistoriska riksmuseet (Swedish Museum of Natural History), Stockholm. They comprise more than 4500 plant remains. Plant fossils were collected over a long time span by different collectors (Denk et al., 1999). The material was actively studied by Oswald Heer, who published on the Spitsbergen fossil flora between 1866 and 1883. Since then, only a handful of palaeobotanists have worked with fossil plants from this area (e.g. Renault, 1900; Schloemer-Jäger, 1958; Manum, 1962; Zastawniak, 1981; Budantsev, 1983; Kvaček et al., 1994; Uhl et al., 2007; Budantsev and Golovneva, 2010). The majority of Spitsbergen megafossils are leaves, and leaves also make up the bulk of floral diversity. The flora is clearly dominated by angiosperms, including species from the families Cercidiphyllaceae, Ulmaceae, Fagaceae and Betulaceae. Most of them are imprints yielding no cuticle; fruiting and flowering parts are generally rare and in a state of preservation that renders them unidentifiable. Unlike many collections that were collected Table 1 Floral composition and insect damage types for the ‘pooled samples’ of the Firkanten Formation; the term ‘pooled sample’ refers to all the leaves sampled from a stratigraphic level, including several localities (compare Table S1). DT, damage type. Species§

Leaves # DTs⁋

Acer arcticum Alnus kefersteinii Betula sp. Celastrinites septentrionalis Fagales gen. et sp. indet.

8 2 34 19 138

0 1 5 7 10

0 50.0 20.6 47.3 15.2

1 3 23 24 6

1 0 8 4 2

100.0 0 56.5 20.8 16.7

131

10

16.0

1 4 10 1

0 1 4 0

0 25.0 50.0 0

1

0

0

2 8 2 10 59 6

0 0 0 3 8 3

0 0 0 30.0 32.2 50.0

12,33,34 1,2,8,11,12,13,16,32 2,12,34

10

2

20.0

1,2

51 20 5 4 45

6 6 0 0 4

23.5 35.0 0 0 15.6

2,11,12,32,34,80 1,2,4,5,12,16

629

26

21.9

1,2,3,4,5,8,11,12,13,14, 15,16,25,30,31,32,33, 34,37,43,57,60,62,63, 78,80

cf. Hamamelidaceae “Cornus” hyperborea Corylites hebridicus “Corylites” sp. Craspedodromophyllum spp. div. Dicot. sp. indet. Dicotylophyllum ssp. div. Fagopsis groenlandica Grewiopsis pterospermoides Juglandaceae gen. et sp. indet. “Majanthemophyllum” boreale Nordenskioeldia borealis Platanus sp. Populus richardsonii Rarytkinia quercifolia Trochodendroides richardsonii Trochodendroides richardsonii subsp. arctica Trochodendroides richardsonii subsp. crenulata Trochodendroides sp. Trochondendroides crenulata Ulmites ulmifolius Viburnum whymperi Zizyphoides flabellum Total:

% Damage

Damage types

2 2,4,12,16,64 1,2,5,8,11,12,32 2,4,12,14,15,16,30, 33,57,80 12 2,4,11,12,32,43,62,78 12,15,16,33 2,12 1,2,3,8,12,25,31,37, 60,80 12 2,12,34,78

2,12,14,15

§ Genera in quotations were assigned based on their original descriptions and are in need of taxonomic revision. ⁋ From Labandeira et al. (2007) and subsequent additions in preparation.

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Table 2 Floral and insect damage composition for the ‘pooled sample’ from the Aspelintoppen Formation; the term ‘pooled sample’ refers to all the leaves sampled from a stratigraphic level, including several localities (compare Table S1). DT, damage type. Species§

Leaves # DTs⁋

Acer arcticum 1 Aesculus longipedunculus 14 Betula sp. 10 Fagales gen. et sp. Indet. 119 cf. Ulmaceae 20 Corylites hebridicus 23 “Corylites” sp. 32 Craspedodromophyllum 3 spp. div. Dicot. sp. indet. 43 Dombeyopsis lobata 1 Grewiopsis pterospermoides 29 “Macclintockia” tenera 1 Platanus sp. 5 Rarytkinia quercifolia 53 Trochodendroides crenulata 43 Trochodendroides richardsonii 33 Trochodendroides richardsonii 5 subsp. arctica Trochodendroides richardsonii 7 subsp. crenulata Trochodendroides sp. 4 Ulmites ulmifolius 29 Zizyphoides flabellum 4 Total:

479

% Damage

Damage types

0 0 2 7 4 4 2 0

0 0 0.4 9.2 25 30.4 9.4 0

3 0 2 0 2 7 3 5 2

6.9 0 6.9 0 20.0 24.5 18.6 27.3 40.0

2

42.9

2,56

0 4 0

0 13.8 0

2,12,14,16

22

15.7

12,41 2,4,12,33,44,53,94 1,2,15,163 2,3,12,80 2,12

2,25,80 2,4 12,44 2,4,5,7,12,13,44 2,12,32 1,2,3,52,56 12,32

1,2,3,4,5,7,12,13,14,15, 16,25,32,33,41,44,52, 53,56,80,94,163

§

Genera in quotations were assigned based on their original descriptions and are in need of taxonomic revision. ⁋ From Labandeira et al. (2007) and subsequent additions in preparation.

more recently, the historical Spitsbergen collection housed at the Swedish Museum of Natural History appears not to be biased to more complete and better preserved specimens. In contrast, there is a great number of fragmentary specimens. At the same time, in the original accounts on the floras from Spitsbergen, the number of recognised taxa appears to be much too high (e.g. Denk et al., 1999; Budantsev and Golovneva, 2010). For this study fossil leaf assemblages were quantitatively studied from several Tertiary deposits in the Central Basin and Calypsostranda Graben (Fig. 1; Tertiary deposits; Dallmann et al., 1999). A total of 629 leaves (27 dicot species) were analyzed from the Paleocene Firkanten Fm., 479 leaves (20 species) from the younger Aspelintoppen Fm., and 459 leaves (26 species) from the Late Eocene to Early Oligocene Renardodden Flora (see Tables 1–3 and supplementary material in Appendix A), located during the Palaeogene at a palaeolatitude of ~68–73°N (see Smith et al., 1994). At each census site, every morphologically identifiable, non-monocot angiosperm leaf (or leaflet in case of compound leaves) with more than half of the blade intact was scored for the presence/absence of 35 insect-feeding morphotypes (Labandeira et al., 2007) (Fig. 2). These damage types (DTs) can be further classified into seven functional feeding groups (FFG): hole feeding (HF), margin feeding (MF), skeletonization (S), surface feeding (SF), galling (G), mining (M), and piercing and sucking

Table 3 Floral and insect damage composition for the ‘pooled sample’ from the Renardodden Flora; the term ‘pooled sample’ refers to all the leaves sampled from a stratigraphic level, including several localities (compare Table S1). DT, damage type. Species§

Leaves

# DTs⁋

% Damage

Damage types

Acer arcticum

154

11

21.4

1,2,4,5,12,13,16,25, 41,43,90

2 2 1 32 1 7 3 42 5 9 72 12 1 1 1 1 11 7 2 1 29 24

0 0 0 3 0 1 0 7 1 1 2 3 0 0 0 0 3 1 1 0 2 5

0 0 0 15.6 0 14.3 0 28.6 20.0 22.2 2.8 41.7 0 0 0 0 27.3 14.3 50.0 0 6.9 33.3

16 1 4 18

2 0 1 2

18.75 0 25.0 5.6

459

18

17.6

Acer spitsbergense Betula sp. Celastrinites septentrionalis Fagales gen. et sp. indet. cf. Ulmaceae Cornaceae gen. et sp. indet. “Cornus” hyperborea Corylites hebridicus “Corylites” sp. Craspedodromophyllum spp. div. Dicot. sp. indet. Dicotylophyllum spp. div. Domebeyopsis sp. Juglandaceae indet. “Macclintockia” tenera Nyssidium arcticum Platanus sp. Populus richardsonii Rarytkinia quercifolia “Tilia” malmgrenii Trochodendroides richardsonii Trochodendroides richardsonii subsp. crenulata Trochodendroides sp. Ulmites ulmifolius Viburnum nordenskioeldii Zizyphoides flabellum Total:

2,3,12 43 2,12,15,16,25,33,80 1 12 2,16 12,43,44

2,4,33 2 12 14,34 2,4,12,25,34 12,43 2,34

1,2,3,4,5,12,13,14, 15,16,25,33,34,41, 43,44,80,90

§ Genera in quotations were assigned based on their original descriptions and are in need of taxonomic revision. ⁋ From Labandeira et al. (2007) and subsequent additions in preparation.

(PS), as described elsewhere (Labandeira et al., 2002b, 2007). The complete census data are available in the Appendix and include 1567 leaves. Palaeoclimate proxies for the Palaeogene of Spitsbergen were investigated by Golovneva (2000) and Uhl et al. (2007). Their results indicate a drop of mean annual temperature (MAT) from the Paleocene Firkanten Fm. to the Aspelintoppen Fm., whereas there are no great differences between the palaeoclimate proxies of the Aspelintoppen Fm. and Renardodden Flora (Table 4). While Golovneva (2000) did not find evidence for a substantial decrease in mean annual precipitation (MAP), based on a CLAMP analysis, she suggested that the temperature of the coldest month had decreased drastically during deposition of the Firkanten Fm. and the younger floras (Table 4). This would suggest increased seasonality for these floras. It is important to note, however, that none of these studies did consider the possible effect of different depositional environments in the Firkanten Formation versus the Aspelintoppen Formation and the Renardodden Flora on the inferred palaeoclimate (see Section 2.1). Quantitative analyses of insect damage were done using R version 2.9.2 (www.r-project.org). In damage diversity analyses, sample

Fig. 2. Representative insect damage on the early Tertiary Spitsbergen flora. A. Extensive margin feeding (arrows) on ‘Ulmites’ ulmifolius (S052095-01; DT12, 14). B. Cuspate margin feeding (arrow) on ‘Corylites’ hebridicus (S052198, DT12). C. Medium-sized, circular perforations (arrows) on ‘Betula’ sp. (Betulaceae) (S051828; DT2, 4). D. ‘Corylites’ hebridicus with oval-shaped feeding holes between secondary veins (S051862-04, DT12). E. Full-depth serpentine mine (white tracing line) deployed as broadly looping swaths that cross all major veins on Fagales gen. et sp. indet. (S052214-01; DT94). F. Secondary-vein associated skeletonization on Acer arcticum (Sapindaceae) with poorly developed reaction rim (S050877; DT16), and G. Skeletonization on katsura tree leaf (Cercidiphyllaceae: Trochodendroides sp.) (S051653-01; DT16). H. Long serpentine mine with undulatory frass on Rarytkinia quercifolia (Fagaceae) (S052042; DT44). I. Detail of mine in H. J. Detail of structurally similar, undiagnostic, circular galls occurring on the edge of the leaf on Fagales gen. et sp. indet. (S052383; DT33). K. Structurally similar, undiagnostic, circular to ellipsoidal galls occurring on the leaf blade ‘Corylites’ hebridicus (S052169-01; DT80). L. Detail of galls in K. M. Circular, thick gall that is 1 to 2.5 mm in diameter and that occurs throughout the leaf on cf. Ulmaceae (Ulmaceae) (S052163-02; DT163). N. Detail of galls (arrows) in M. O. Pattern of hole feeding in intercostal areas on ‘Corylites’ hebridicus (S050828-01; DT2). P. Detail of mine in E. Front-slashed scale bars = 10 mm; striped scale bars = 5 mm; dotted scale bars = 1 mm.

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Table 4 Insect damage composition for the three stratigraphic levels of plant bearing formations considered in this study from the Tertiary of Spitsbergen. MAT, mean annual temperature; MAP, mean annual precipitation; CMMT, cold-month mean temperature; DT, damage type; Spec. Dam., specialized damage. Formation/Flora

MAT, °C⁑

MAP (cm)

CMMT, °C⁑

Plant Diversity at 400 leaves⁋

No. of DT

DT at 400 leaves✝

Renardodden

8.4 ± 1.8a 8.8 ± 1.2b 9.5 ± 1.8a 9.0 ± 1.2b 12.6 ± 1.8a 10.9 ± 1.2b

124.3 ± 43b

− 1.0 ± 3.3b

Aspelintoppen Firkanten ⁑ a b ⁋ ✝ §

171.6 ± 43

b

182.6 ± 43

b

Spec. Dam at 400 leaves✝

Mines at 400 leaves✝

% Mines§

Galls at 400 leaves✝

% Galls§

25.9 ± 1.0

18

16.8 ± 0.9

8.3 ± 0.8

1.9 ± 0.8

0.5 ± 0.6

5.5 ± 0.6

3.7 ± 0.7

1.5 ± 3.3

b

20.8 ± 0.7

22

19.7 ± 1.3

10.6 ± 1.0

2.7 ± 0.5

1.0 ± 0.5

4.5 ± 0.7

1.7 ± 0.6

6.5 ± 3.3

b

26.7 ± 1.3

26

21.6 ± 1.6

10.3 ± 1.3

3.6 ± 0.6

2.2 ± 0.7

2.8 ± 0.4

1.3 ± 0.5

Errors are ± 1σ. Palaeoclimate estimates obtained with CLAMP (Climate Leaf Analysis Multivariate Program) from Golovneva (2000). Palaeoclimate estimates obtained with CLAMP (Climate Leaf Analysis Multivariate Program) from Uhl et al. (2007). Error represents Heck et al. (1975) standard error. Error represents one standard deviation above and below the mean of the resample. Error represent ± 1σ, based on a binominal sampling distribution.

size was standardized by selecting random subsets of leaves without replacement and calculating the damage diversity for the subsample (as per Wilf et al., 2001). This process was repeated 5000 times, and the results were averaged to obtain the standardized damage diversity for each flora. The standard deviations (SD) for the resamples were calculated to provide sample error bars. The same procedure was used also to standardize insect damage diversity to 25 leaves on each of the 16 species–site pairs with at least 25 specimens (Fig. 4). The host species means were also combined into floral grand means. Analysis of variance (one-way ANOVA), was applied to compare insect damage diversity data for single formations and/or localities through time. Assemblage structure, based on proportional data within the functional feeding groups (FFG's), was analyzed for the Spitsbergen formations and/or sites and latitudes, including also data from the French paratropical mid-latitude locality Menat (Wappler et al., 2009), using a G-test. 4. Results 4.1. Damage frequency and diversity Insect damage censuses were conducted for three plant bearing sedimentary rock formations (see Fig. S1 in supplementary material in Appendix A) and variations for insect damage diversity on herbivorized dicot leaves for bulk floras between the different formations are illustrated in Fig. 3. Overall, the percentage of folivory was significantly different between the formations (F[1,4] = 7.70, P b 0.001). Total folivory was 21.68 ± 1.70% in the Firkanten Fm., 19.77 ± 1.34% in the Aspelintoppen Fm., and 16.84 ± 0.98% in the Renardodden Flora (Table 4). Like the frequency data, the bootstrap curves indicate greater damage diversity for the Paleocene plant bearing Firkanten Fm. The number of DT occurrences within the seven FFG was compared among the three formations using a G-test. DT's from all FFG's except piercing and sucking were found in all formations: the piercing and sucking damage was only observed in the Renardodden Flora The total number of DT occurrences within each FFG did differ significantly through the study interval (GFFG[12] = 27.55, P = 0.006), indicating a recognizable response of high-latitude ecosystems to changing environments during the study interval (Fig. 3; Table 4). Nevertheless, traces indicating specialized feeding, particularly galling, mining, or piercing and sucking are rare, whereas traces formed by external foliage feeders are common. Damage diversity on indiviual dicot host plant species is shown in Fig. 4. Damage frequency and diversity are significantly correlated (r2 = 0.792, P b 0.001, n = 16, damage diversity values at 25 bootstrapped specimens). In contrast, the measures on damage diversity versus feeding group richness are not well correlated among hosts (Spearman rank-order correlation coefficient: S = 366, P = 0.073, rS = 0.46), indicating a higher variance in herbivory webs rather than guilds or

Fig. 3. Rarefaction curves for insect damage diversity on herbivorized dicot leaves for bulk floras, from Me (Menat, S-France), Fir (Firkanten Fm., Svalbard), Asp (Aspelintoppen Fm., Svalbard), and Rd (Renardodden Flora, Svalbard). Curve endpoints are enlarged to increase visibility of seperated curves. Curves for Menat have no endpoint depicted because terminating outside the graphed area. Data for Menat is taken from Wappler et al. (2009). Error bars representing one standard deviation above and below the mean of the resamples.

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Fig. 4. Resampled, rank-ordered insect-feeding diversity on individual dicot host plant species with ≥ 25 total specimens at each site. For each species, the mean is shown (+1σ). A. Damage frequency. B. Damage types. Note: Damage frequency depends on the abundance and density of insects in an area (Coley, 1998).

feeding groups (Simberloff and Dayan, 1991; Wilf et al., 2005; Fontaine et al., 2009). For example, the Renardodden sample reaches 5.77 of the 6 possible feeding grous (excluding piercing and sucking since these were only encountered in the Renardodden Flora) at 50 leaf specimens, whereas the Aspelintoppen sample reaches this value at 260, and the Firkanten sample at 580 leaf specimens. Therefore, increasing feeding groups, may reflect an in situ diversification and accommodation to many of the dominant floral elements (e.g. Acer, Ulmus, Aesculus; Denk et al., 1999) in the younger limnofluvial deposits. Variations in composition through time reveal the particular relationships between host plants and insect herbivores and illustrate changes in the importance of different damage types or functional feeding groups, whereas damage frequency additionally depends heavily on the abundance and density of insect populations (e.g. Coley, 1998; Currano, 2009). Among the heavily herbivorized leaf species within the Firkanten and Aspelintoppen formations are species of Trochodendroides (Cercidiphyllaceae) with 31 to 33% of leaves externally damaged (Table 1–2). For the Late Eocene to Early Oligocene Renardodden Flora, external damage is moderately high on Acer arctium Heer (21% of the leaves damaged) and Corylites hebridicus Seward and Holttum (26%) (Table 3). The Firkanten and Aspelintoppen Formations have the greatest number of species with abundant specialized damage. In particular, our data suggest an increase in galling and a decrease in mining activity through the study intervals (Table 4). Galling is most

abundant within the Renardodden Flora; 3.7% of the leaves show galling structures. Galls occcur on nine species. Trochodendroides sp. (7.8% of leaves galled) and Corylites hebridicus Seward and Holttum (17.4% of leaves galled) were attacked by a larger diversity of gallinducing insects, whose traces include 4 of the 6 galling types found in the Renardodden Flora. Most of the galls are morphologically similar and represent mainly taxonomically undiagnostic circular to ellipsoid galls that occur on the leaf lamina or on veins. The galling frequency in the Late Paleocene sites decreases below 1.3% with only 6 galling occurrences. The increase in galling from the older to the younger formations is accompanied by a decrease in mining. Mining is most abundant in the Firkanten Fm., where 2.2% of the leaves are mined. In the younger stratigraphic levels b1% of leaf-mining damage was encountered. The highest number of leaf-mining damage types within the Firkanten Fm. occurs on Acer arcticum. Although only 2.6% of the leaves are mined, the mines comprise 75% of all damage types recorded for the Late Paleocene sedimentary rock formation. In addition, mining occurs on three other species: Corylites sp.’, Dicotylophyllum sp., and Trochodendroides sp. Generally, the mining frequency within the Late Paleocene sites is significantly higher than at the Late Eocene–Early Oligocene sites (t = 1.75, d.f. = 28, p = 0.04). The mining damage types are similar to those made by lepidopterans, and all host plants show mine characteristics of the Gracillarioidea clade (DT41-44, 90). Today, Gracillaroidea leaf-mining moths (e.g. Phyllocnistinae) are especially speciose on Fagales, about half the known host records being from this group (Lopez-Vaamonde et al., 2003; Lopez-Vaamonde et al., 2006).

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Plant ecological traits, such as leaf size or secondary metabolites also potentially influence the observed pattern. Digital measurements on the species leaf area (mean natural log) indicate a decrease in leaf size through the study interval (r 2 = 0.594, P = 0.04, n = 220), which also significantly correlates with the consumed leaf area through the study interval (r 2 = 0.928, P = 0.010, n = 220). Leaf size also correlates significantly with damage diversity (at 25 specimens) only within the Renardodden Flora (r 2 = 0.893, P b 0.001, n = 4). There was no such correlation evident for the other formations (Firkanten Fm., r 2 = 0.052, n = 5; Aspelintoppen Fm., r 2 = 0.025, n = 7). 4.2. Damage on individual hosts During the early Tertiary, warm, humid climates at high latitudes allowed broadleaved deciduous forests (as defined by Wolfe, 1985) to flourish north of the Arctic Circle. Therefore, tracing insect damage on single plant taxa can show if changes in damage composition through time are caused by changes in plant composition (floral turnover) or if damage diversity correlates with changing temperatures or changing leaf traits. Two plant taxa, Fagales gen. et spec. indet. and

Trochodendroides richardsonii match the criteria (see Material and methods), and are present in all formations (Fig. 5). Trochodendroides richardsonii shows the same general pattern as observed for the pooled samples of each formation (Fig. 3). There is a steady decrease of damage frequency and diversity from the Firkanten Fm. to the Late Eocene to Early Oligocene Renardodden Flora, whereas the decrease is more pronounced in the younger strata than between the Paleocene to Eocene sites (Fig. 5A, B). Complementing the pattern seen for the leaf size data, herbivory frequency on T. richardsonii correlates significantly with decreasing leaf size (mean natural log) (r 2 = 0.464, P = 0.05, n = 33). As in T. richardsonii, Fagales gen. et spec. indet. generally reflects the trend seen elsewhere in herbivory through time for specialized damage diversity and frequency. However, Fagales gen. et spec. indet. showed increased total damage frequency and diversity from the Aspelintoppen Fm. to the Renardodden Flora reaching herbivory levels previously recorded for sites of the Middle Paleocene Firkanten Fm. (Fig. 5E, F). FFG diversity graphs for both host plants Fagales gen. et spec. indet. and T. richardsonii show a different trend than the total damage frequency and diversity data . Within the youngest formation, higher

Fig. 5. Insect damage on single plant taxa. A. Total (circles) and specialized (diamonds) damage frequency on Trochodendroides richardsonii (Heer) for each stratigraphic level with at least 25 leaves. Error bars represent ± 1σ, based on a binominal sampling distribution. B. Total (circles) and specialized (diamonds) damage diversity on T. richardsonii (Heer) standardized to 25 leaves, with error bars representing one SD ± the mean of the resamples. C. Galling diversity on T. richardsonii (Heer) standardized to 25 leaves, presented as in (B). D. Functional Feeding Group (FFG) diversity on T. richardsonii (Heer) standardized to 25 leaves, presented as in (B). E. Total and specialized damage frequency on cf. Fagales. Errors as in (A). F. Total and specialized damage diversity on cf. Fagales, presented as in (B). G. Galling diversity on cf. Fagales, presented as in (B). H. FFG diversity on cf. Fagales, presented as in (B).

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FFG diversity values than for the older formations are found (25 bootstrapped specimens; Fig. 5D, H). Variations in composition through time reveal the particular relationships between host plants and insect herbivores and illustrate changes in the importance of different damage types or functional feeding groups (e.g. Currano et al., 2010).

4.3. Damage type richness along the latitudinal gradient Here we compared the similarity in functional feeding guild structure, the DT composition and occurences between the (later) Early to Middle Paleocene Firkanten Fm. (Spitsbergen, Norway) and the mid-latitude Middle Paleocene locality Menat (France) using the Sørensen diversity index (Sørensen, 1948). The value will be close to 1 for sites that have most of their DT in common and close to 0 for very dissimilar sites. The total number of DT occurences observed is significantly lower at Spitsbergen during the Paleocene than at Menat (GFFG[6] = 19.39, P = 0.003). For all DT's, the presence/absence measure (Sørensen Incidence similarity index), with a value of 0.585 is unexpectedly high, contrary to the expectation that the similarity of herbivorous insect assemblages between such long-distance LTG's would decrease towards lower latitudes (but see Archibald et al., 2011). Floral grand means of the host data in Fig. 4 show that the Menat species have more damage types and feeding groups than the three pooled Palaeogene Spitsbergen formations (Fig. 6), indicating greater richness of plants and greater community diversity of insects within lower latitude communities than at the high-latitude sites. Since the similarity of herbivorous insect assemblages decreases towards lower latitudes, such a pattern would be expected (e.g. Rosenzweig and Sandlin, 1997; Koleff et al., 2003; Novotny et al., 2006; Dyer et al., 2007).

Fig. 6. Grand means for the resampled species means (shown in Fig. 4) of insect damage diversity, ± 1 standard error of the mean. Data for Menat is taken from Wappler et al. (2009). N, Number of species in the sample. Black circles and left scale, damage types (DT); gray squares and right scale, functional feeding groups (FFG). Asterisks next to early Tertiary Spitsbergen localities grand means indicate significance (one-way ANOVA) of comparison with corresponding Menat grand means.

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5. Discussion Palaeoclimate estimates for the early Tertiary floras of Spitsbergen and adjacent areas point to a slight cooling trend with decreasing coldmonth mean temperature and growing season precipitation (GSP) from the Middle Paleocene to the Late Eocene (to Early Oligocene (Golovneva, 2000; Uhl et al., 2007; Eldrett et al., 2009; Budantsev and Golovneva, 2010; 2010; Eberle et al., 2010; Greenwood et al., 2010). Also globally averaged δ 18O temperatures for an ice-free ocean for the time intervals investigated here (Middle Paleocene, Late Eocene to Early Oligocene) suggest a cooling from 8 °C to b 6 °C (Zachos et al., 2001). This is in agreement with the here reported decrease in insect damage diversity, frequency, and insect population density in the course of the Palaeogene (Figs. 3–4, 6). In general, insect damage encountered in the Tertiary floras of Spitsbergen comprises mainly external foliage feeding, whereas specialized feeding behaviours, such as galling, mining or piercing and sucking are extremely rare (Fig. 2; Table 4). The more frequent occurrence of galling in the younger formations is in agreement with the inferred decrease of growing precipitation in these formations. At present, galling is mainly found in relatively dry temperate and subtropical (including Mediterranean) regions of the world (Price et al., 1998). This may be a weak indication for more pronounced seasonality in precipitation during the Late Eocene (to Early Oligocene; see also Sluijs et al., 2009). Although the observed changes in leaf physiognomic types and insect herbivory are in agreement with evidence from deep sea isotopes, one should also keep in mind that the Firkanten and Aspelintoppen formations were deposited under different depositional settings (see also Section 2.1). The plant bearing sediments of the Firkanten Formation were deposited in alluvial plains with minor marine influence in landscapes that consisted of a mosaic of bogs, boggy forests, marshlands, and hammocks (Schweitzer, 1974; Steel et al., 1981; Denk et al., 1999). In contrast, depositional environments of the Aspelintoppen Formation are characterized by higher sedimentation rates and reflect tectonic uplift (Steel et al., 1981). According to Schweitzer (1974), extensive lowland and upland forests alternated with relatively large shallow lakes. Hence, the observed changes in temperature, growing season precipitation and seasonality may also reflect different environments (e.g. Danks, 2004). Environmental variables influence insect population size, insect metabolism and development time, plant defense mechanisms and diversity, which in turn could have had an impact on herbivory frequency and diversity (e.g. Murdoch et al., 1972). Biogeographic theory predicts that greater herbivory generally occurs in the tropics than in temperate regions. Specifically, a greater diversity of plants appears to cause a greater community diversity of insects in lower latitudes (e.g. see discussions in Novotny et al., 2006, Dyer et al., 2007 and references therein). Understanding the factors causing this pattern is a central question in ecological, evolutionary, and palaeobiological research (e.g. Coley and Aide, 1991; Bolser and Hay, 1996). Several qualitative climate reconstructions indicate generally warmer conditions throughout the Palaeogene on the continents even at higher latitudes (e.g. Robert and Kennett, 1994; Francis and Poole, 2002; Eldrett et al., 2009). Thus, proxy data indicate a latitudinal thermal gradient (LTG) that was less pronounced than the gradient simulated by climate models (e.g. Shellito et al., 2003; Fricke and Wing, 2004; Shellito and Sloan, 2006; Archibald et al., 2010; Rose et al., 2011), a feature which seems to be characteristic of periods with greenhouse climates (e.g. Huber et al., 1995), often associated with lowered seasonality and mild winters lacking frost days (e.g. Markwick, 1994; Greenwood and Wing, 1995; Markwick, 1998). During larger global hyperthermal events linked to the injection of greenhouse gasses into the atmosphere from sedimentary reservoirs, Arctic MAT may have increased by 5–10 °C to perhaps approximately 23 °C, with the coldest month mean temperature greater than 8 °C at approximately 85° N palaeolatitude (e.g. Sluijs

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Table 5 Floral diversity and damage diversity. DT, damage type; N, number of leaves in the census; S, the total number of plant species. Data for Genera and S for Svalbard formations from Tables 1 to 3 and Budantsev and Golovneva (2010; in rectangular brackets). Floral diversity data for Menat from Wappler et al. (2009). Locality/formation/flora

N

Menat Firkanten Formation (syn. Barentsburg Formation) Aspelintoppen Formation (syn. Storvola Formation) Renardodden Flora

938 52 629 23[17]

76 60.8 28[20] 26.7

2.7 1.3

39 26

479 16[16]

21[20] 21.5

0.7

22

459 23[16]

27[21] 25.9

1.0

18

§ ⁋

# S Genera

Div. at Div. # 400 leaves§ error⁋ DT's

Diversity was rarefied to 400 leaves using analytical rarefaction. Error represents Heck et al. (1975) standard error.

et al., 2009; Archibald et al., 2011). A shallow early Palaeogene temperature gradient (MAT, cold-month mean temperature, growing season precipitation; see Table 4) is also consistent with occurences of crocodilians or palms (Schweitzer, 1980; Markwick, 1998; Sluijs et al., 2009) and subtropical to tropical plant communities at latitudes much higher than their present northern limits. That in turn could have allowed herbivorous insects to migrate polewards with a changing climate, where species richness and herbivorous feeding pressure increased (e.g. Willig et al., 2003; Parmesan, 2006; Dyer et al., 2007; Adams et al., 2010; Netherer and Schopf, 2010; Archibald et al., 2011). This is in stark contrast to the contemporary Middle Paleocene fossil-lagerstätte Menat, France, where diverse insectfeeding damage on a large number of plant species was found (Wappler et al., 2009) (Fig. 6; Table 5). Apparently, specialized feeding behaviour is more frequent in highly diversified plant communities (providing a large number of niches to herbivorous insects) than in moderatley diversified communities as found in the Palaeogene of Spitsbergen (Table 6). To date, a number of variables, including temperature (Wilf and Labandeira, 1999; Wilf et al., 2001; Bale et al., 2002; Currano et al., 2008), precipitation (Marquis and Braker, 1994; Wright and Samways, 1998; Givnish, 1999; Wilf et al., 2001; Price and Hunter, 2005), resource limitation (Coley et al., 1985; Labandeira et al., 2002a; Fine et al., 2004; Wappler et al., 2009), and changing patterns of seasonality (Archibald et al., 2010) have been found to cause these variations. The developmental success of insect herbivores also indirectly depends on climate, as environmen-

tal parameters impact on plant physiology. Thus, the highest peaks of herbivory would appear to be expected when temperature and humidity were high (Firkanten Fm.), because populations of herbivores build up during the wet season (Coley, 1983; Aide, 1993; Price and Hunter, 2005). Therefore, it has also been hypothesized that in modern lowland forests, timing of foliation has shifted towards the dry season when insect herbivores are fewer in number (Coley, 1983; Aide, 1988, 1992). Furthermore, there is also an increase of small-leaved host plants from the older Firkanten Formation to the younger Aspelintoppen Formation. In particular, leaves in the Firkanten Fm. localities are comparatively larger, some exceeding ~ 30 cm in length (Kvaček et al., 1994; Birkenmajer and Zastawniak, 2005; Uhl et al., 2007), whereas smaller leaves might have been less prone to insect damage and may have been an important defense strategy (e.g. Moles and Westoby, 2000; Wilf et al., 2001). Then again larger leaf size may be indicative of a climate with high precipitation and/or an adaptation to low angles of sun ligth at high latitudes (e.g. Burnham and Johnson, 2004; Greenwood et al., 2010). The overall reduced damage frequency and diversity in the Spitsbergen flora as compared to mid-latitude floras reflects the general picture that plant–insect interactions vary geographically (e.g. Futuyma and Mitter, 1996; McGlynn et al., 2010 and references herein). Variations in extant insect herbivory along latitudinal and climatic gradients have been observed, and greater herbivory generally occurs in the tropics than in temperate regions (Coley and Barone, 1996; Price et al., 1998). One possible explanation, apart from the substantially larger plant diversity in the tropics, could be that boreal and temperate plant species (e.g. Fagaceae) often contain significant concentrations of secondary metabolites that are important for the regulation of herbivory and herbivore abundance (e.g. Haukioja, 1980; Jeffries et al., 1994; Graglia et al., 2001). In particular, the vitality status and stress situation of plants influence secondary metabolism and in this way resistance to insect infestation and nutritional quality (palatability) of foliage. Furthermore, there is a general consensus in ecology that the diversity of insect herbivores is strongly related to the diversity of host plants (e.g. Siemann et al., 1998; Knops et al., 1999; Hawkins and Porter, 2003; Novotny et al., 2006; see also Table 5). On the other hand, relatively little is known about the specific mechanical properties that deter herbivores (e.g. Lucas et al., 2000; Siska et al., 2002) but there is a strong negative association between leaf

Table 6 Fossil insects known from Svalbard compared to the functional feeding groups recorded in the Svalbard flora, and their fagalean host-plant affiliation. Below the dashed line, insect clades are listed that were probably present based on the affinities of damage types preserved on the leaf blades. Hole feeding (HF), margin feeding (MF), skeletonization (S), surface feeding (SF), galling (G), mining (M), and piercing and sucking (PS). Insect clade⁎

Hymenoptera Ichneumonidae Coleoptera Carabidae Hydrophilidae Buprestidae Elateridae Throscidae Chrysomelidae Scarabaeidae Lepidoptera Thysanoptera Diptera Hemiptera

Mode of life

Fagalean host plant

Functional Feeding Groups HF

MF

S

X

X

X

X

X

X

X

SF

G

M

X

X

PS

Parasitoids of other insects Mainly carnivorous Larvae are predatory while the adults may be vegetarians or predators in addition to scavenging Larvae bore through roots, logs, stems, and leaves of various types of plants, ranging from trees to grasses Larvae usually saprophagous, but some species are serious agricultural pests, and other species are predators of other insect larvae Larvae mainly feeding on soft, decaying wood Adult and larval leaf beetles feed on all sorts of plant tissue Larvae mostly feeding on soft, decaying wood Larvae are herbivores, but a few are carnivores and detritivores Feeding on a large variety of sources, both plant and animal Feeding on a large variety of sources, both plant and animal Most hemipterans are phytophagous, feeding on plant sap

X

X

X

X

X

X X X X X

X X

X

X

X

X X X X

⁎ Systematic placement of fossil insect remains following the latest revison of Birket-Smith (1977). Twenty-five fossil insect remains are availabale from Svalbard.

X X

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toughness and herbivore damage across species (Coley, 1983). Thus, the longer growing season at low latitudes might require tougher leaves (in order to extend leaf life-span), and increased leaf toughness might reduce palatability to herbivores (e.g. Royer et al., 2007). The leaf floras recorded from early Tertiary sedimentary rocks from Spitsbergen are mainly composed of deciduous broadleaved and coniferous taxa, which would appear to make them more vulnerable to insect damage. At the same time, a relatively species-poor forest vegetation did not allow for a highly diversified insect fauna as observed from coeval fossil plant assemblages at low latitudes (e.g. Wilf, 2008; Adams et al., 2009; Wappler et al., 2009; Archibald et al., 2010). 6. Conclusions This study reports for the first time a wealth of insect traces on early Tertiary leaves from the Arctic Area. The high abundance of large deciduous leaves in the fossil assemblages of Spitsbergen suggests that these leaves were particulary prone to insect damage. At the same time, the relatively low insect diversity recorded may be due to the low number of tree taxa in the high-latitude forests of Spitsbergen. The observed decline in insect herbivory from the Early Paleocene to the Late Eocene/Early Oligocene in Spitsbergen is attributed to decreasing temperatures (MAT, cold-month mean temperature) and a less diverse insect fauna rather than to leaf phenology (as seen in Trochodendroides richardsonii). Furthermore, the present observations of fossil plant–insect interactions are consistent with estimates of ‘simpler’ trophic level structures in the early Tertiary Arctic than in coeval mid-latitude ecosystems (e.g. Archibald et al., 2010), where the abundance of phytophagous insects relative to plant biomass is high and highly spezialized phytophagous insect groups such as gallers and leaf miners are common. Acknowledgements We would like to thank O. Johansson, and A. Lindström for assistance in the museums collections; and the anonymous reviewers for constructive comments. This research received support from the SYNTHESYS Project (http://www.synthesys.info/) that is financed by the European Community Research Infrastructure Action under the ‘Structuring the European Research Area’ program (to T.W.), grants of the German Science FoundationWA 1492/3-1; 4-1; 6-1 (to T.W.), and the IPEV-SPITZP3 1005 Project/Expedition. Appendix A. Supplementary data Supplementary data to this article can be found online at doi:10. 1016/j.palaeo.2011.07.020. References Abbott, R.J., Brochmann, C., 2003. History and evolution of the arctic flora, in the footsteps of Eric Hultén. Molecular Ecology 12, 299–313. Adams, J.M., Zhang, Y.J., Basri, M., Shukor, N., 2009. Do tropical forest leaves suffer more insect herbivory? A comparison of tropical versus temperate herbivory, estimated from leaf litter. Ecological Research 24, 1381–1392. Adams, J.M., Brusa, A., Soyeong, A., Ainuddin, A.N., 2010. Present-day testing of a paleoecological pattern: is there really a latitudinal difference in leaf-feeding insect-damage diversity? Review of Palaeobotany and Palynology 162, 63–70. Aide, T.M., 1988. Herbivory as a selective agent on the timing of leaf production in a tropical understory community. Nature 336, 574–575. Aide, T.M., 1992. Dry season leaf production: an escape from herbivory. Biotropica 24, 532–537. Aide, T.M., 1993. Patterns of leaf development and herbivory in a tropical understory community. Ecology 74, 455–466. Archibald, S.B., Bossert, W.H., Greenwood, D.R., Farrell, B.D., 2010. Seasonality, the latitudinal gradient of diversity, and Eocene insects. Paleobiology 36, 374–398. Archibald, S.B., Johnson, K.R., Mathewes, R.W., Greenwood, D.R., 2011. Intercontinental dispersal of giant thermophilic ants across the Arctic during early Eocene

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