Pollen and non-pollen palynomorph depositional patterns in Kaziranga National Park,India: Implications for palaeoecology and palaeoherbivory analysis

Abstract

The main aim of this study is to produce a modern analog for pollen and non-pollen palynomorphs (NPPs) preserved in soil in relation to the different vegetation types and herbivore impact in the Kaziranga National Park (KNP). The pollen data obtained reflects both the extant vegetation types in each habitat as well as landuse, but some site-by-site variation was observed with respect to the coprophilous fungal spores present in the palynoassemblage. Canonical correspondence analysis (CCA) analysis of pollen data reveals the presence of five significantly different vegetation types, while the non-pollen palynomorphs are relatively similar in relation to the different vegetation types. The long-term association of the wildlife and their impact on different vegetation types is one of the main reasons for the variation seen in the depositional pattern in the assemblage. The openland area is one of the most important areas for wildlife in the KNP as indicated by the presence of marker pollen and coprophilous fungal spores in the palynoassemblages. Coprophilous fungal spores were most abundant in this vegetation type reflecting the higher density of herbivores. The representation of pollen and coprophilous fungal spores from the swamp samples reflected the overall composition of all vegetation types existing in the KNP. This data can be utilized as a baseline for the interpretation of paleoecological and paleoherbivory studies in other parts of the Indian subcontinent as well as its potential application at a global level.

Keywords

Coprophilous fungal spores herbivores palynoassemblages pollen spectra swamp vegetation types

Introduction

The study of modern pollen rain in relation to different vegetation types is a prerequisite for the interpretation of the past vegetation and climate in a region and how it has changed over time (Bent and Wright, 1963; Bunting et al., 2004; Deng et al., 2006; Gosling et al., 2009; Janssen, 1967; Overpeck et al., 1985; Prentice, 1985; Wilmshurst and McGlone, 2005; Wright, 1967; Xu et al., 2005). The study of the modern pollen rain and extant vegetation in tropical regions is more complex and critical due to high biodiversity and heterogeneity of the pollen preservation on the forest floor and nearby areas, compared to subtropical and temperate vegetation, as documented by the presence and abundance of the major pollen taxa in the pollen assemblages (Bush et al., 2021; Gosling et al., 2018; Mayle et al., 2000). Phenological factors such as the timing of the flowering period and periods of high rainfall, along with pollen production, mode of pollination, and variation in the mode of pollen dispersal influence pollen preservation both on the landscape surface and eventual integration into soils and sediments. However, based on a knowledge of the pollen spectra and how it represents the major associated plant taxa in relation to the different vegetation types, it is possible to differentiate and distinguished the different vegetation types in a region (Gaillard et al., 1994; Guimarães et al., 2017) and as well as the recognition of differences between modern and historic grassland uses (Hjelle, 1999).

There is an increasing global interest in paleoherbivory and paleodietary analysis in relation to palaeoecology during the Quaternary, particularly with respect to possible dietary changes that may have contributed to the extinction of megaherbivores (Barnosky et al., 2004; Rawlence et al., 2016). Many of these studies have been primarily based on pollen and non-pollen palynomorphs, especially changes in the relative abundance of coprophilous fungal spores, preserved in sedimentary profiles and coprolites (Burney et al., 2003; Carrión et al., 2007; Davis and Shafer, 2006; Gill et al., 2009, 2013; Graham et al., 2016; Johnson et al., 2015; Raper and Bush, 2009; Robinson et al., 2005; van Geel et al., 2018).

The presence of coprophilous fungi in sediments and changes in their relative abundance has been used as an indicator not only of the past presence of herbivores, but also to document changes in population sizes and in some cases the extinction of this part of the Pleistocene megafauna (Baker et al., 2013; Etienne et al., 2013; Feranec et al., 2011; Karanth and Sunquist, 1992; López-Vila et al., 2014; Loughlin et al., 2018; Pokharia et al., 2022; Tunno and Mensing, 2017; Van Asperen et al., 2021; Van Geel, 1972; Van Geel et al., 1980; van Geel, 1976; Van Geel et al., 1983; Van Geel, 1978). More recently coprophilous fungi have increasingly been used as a proxy to address questions of pastoral and other human activities (Burney et al., 2003; Cugny et al., 2010; Davis, 1987; Feeser and O’Connell, 2010; Felauer et al., 2012; Gill et al., 2009; Johnson et al., 2015; Kamerling et al., 2017; Miehe et al., 2009; van Geel et al., 2003). When combined with the study of pollen grains, fungal spores, especially of coprophilous fungi that grow on dung of herbivorous animals can provide useful information for understanding the food habits, ecology, diversity, niche partitioning and changes in relative abundance of past herbivorous species in a region (Basumatary et al., 2017, 2019, 2020, 2021; Ebersohn and Eicker, 1992; Ekblom and Gillson, 2010; Pokharia et al., 2022; Tripathi et al., 2019; Velázquez and Burry, 2012). Previously work on the preservation of modern pollen and non-pollen palynomorphs on the modern surface soil related to highland grazing and past land use and other vegetation changes has also been investigated (Ejarque et al., 2011; Henga-Botsikabobe et al., 2020; Loughlin et al., 2021). Since both fungal spores and the pollen grains in the sediments are commonly encountered in the same palynological slide (van Geel et al., 2003), the documentation of fungal spores, especially those of coprophilous fungal spores, along with the pollen grains can be useful to interpret the impact of herbivores in relation to the different vegetation types in a region. As coprophilous fungal spores are dispersed only for a very short distance, they are local in origin (Graf and Chmura, 2006; Johnson et al., 2015) so will accumulate in sediments with pollen grains and are therefore indicators of the local presence of herbivores in relation to the existing vegetation.

While some research has been conducted to understand past vegetation and climate history in relation to the paleoherbivory in national parks in tropical regions of the world (Burbridge et al., 2004; Ekblom and Gillson, 2010), little research has been carried out on modern pollen deposition in relation to the different vegetation types in national parks and wildlife sanctuaries in Asia (Basumatary et al., 2014; Bera et al., 2014; Djamali et al., 2009; Ghosh et al., 2017; Pandey and Minckley, 2019; Setyaningsih et al., 2019; Tripathi et al., 2016). These previous studies have often not recorded the presence of coprophilous fungal spores so cannot be used to determine the presence and abundance of herbivorous animals in the region. In the absence of skeletal remains of these herbivores, coprophilous fungal spores may serve as an important proxy that can be used to reconstruct the palaeoecology of a region with respect to the presence, types and abundance of herbivores and their impact on the local environment, as well as how changes in the vegetation impacts the local wildlife (Basumatary and McDonald, 2017).

The main aim of this study is to document the depositional pattern of pollen and non-pollen palynomorphs in different vegetation types in Kaziranga National Park (KNP) in relation to the types of wildlife present and their impact on the different types of habitat. Determining the degree of representation of the coprophilous fungal spores in the surface soil and sedimentary profiles serves as the primary proxy to trace the relationship between flora and fauna in the region through time. The combination of pollen and non-pollen palynomorphs, especially the abundance of coprophilous fungal spores, is taken into consideration and calibration during the analysis which permits an interpretation of paleoherbivory and palaeoecology. Based on the changes in frequency of coprophilous fungal spores in the sedimentary profile, an analysis is possible to trace the presence, relative abundance over time and eventual decline and extinction of members of the herbivorous mammals in Kaziranga National Park and to correlate the pattern with what is observed in other national parks located in the tropical and temperate region of the globe. Based on the modern palynomorph analogs seen in different regions, the presence and absence of the local arboreal pollen taxa and coprophilous fungal spore in the pollen assemblages provides a means to distinguish the natural forest vegetation, from areas with heavy grazing or modified into cropland in both tropical and temperate regions. The resulting information can serve as a baseline to examine the influence of paleoherbivory on vegetation in the National Park in the past. This also provides for a better determination of the first human occupation along with their domestic livestock in the area and subsequent impact on the flora and fauna.

Study sites

Kaziranga National Park covers an area of around 430 km² and is bordered on one side by the Brahmaputra River (Figure 1). In 1985, KNP was declared a UNESCO World Heritage Site in recognition of its significance as one of the best managed wildlife parks in the world. As such, KNP is one of the best sites in India and certainly for Southeast Asia to observe the long-term interrelation between plants and the indigenous wildlife, as this interrelationship has not been impacted as extensively by human activities and domesticated animals as at other sites in India. The park is within the Indo-Burmese biodiversity hotspot region, a critical corridor for immigration of members of the Indo-Malayan fauna into the Indian subregion. It is also a critical reserve for tropical species, having served as a gene reservoir for these taxa during glacial periods (Tamma and Ramakrishnan, 2015).

Figure 1.

(a) Map showing the study areas and (b) vegetation coverage map of Kaziranga National Park (modified after Das et al., 2014).

Climate and soil

The climate of the region is controlled by the southwest and northeast monsoons. These weather patterns result in hot, humid summers, and cold, dry winters. The temperature ranges from a minimum of 4°C during winter up to 37°C in summer. The relative humidity is very high and ranges between 75% and 86%. The annual rainfall ranges from 1800 to 2600 mm, and annual flooding is common in KNP during the summer. The soil composition varies from site to site and includes sandy loam soil in forests, sandy soil in grassland, and clayey soil in the swamp and water bodies (Das et al., 2014).

Vegetation and wildlife

In general, there are four main types of vegetation in the KNP; tropical evergreen forest, semi-evergreen forest, deciduous forest, grassland and swamp (Champion and Seth, 1968). Alluvial grassland is the most dominant vegetation type (50.6%), followed by woodland (21.8%), openland areas covered by short grasses and other herbaceous associates (7.7%), and eroded land caused by soil erosion and landslides during intervals of high rainfall 11.7% in the national park (Das et al., 2014).

The evergreen forest is generally confined to the areas adjacent to the Brahmaputra River, small rivers, and streamlets within the park. This vegetation remains evergreen throughout the year in the core regions and is dense and composed of forest elements including Castanopsis indica, Cinnamomum bejolghota, Duabanga grandiflora, Elaeocarpus robustus, Toona ciliata, Mesua ferrea, Symplocos paniculata, Terminalia myriocarpa, Schima wallichii, and Litsea monopetala. The common climbers are Calamus erectus, Vitis latifolia, Paederia foetida, Cardiospermum halicacabum, Trichosanthes dioca, Smilax ovalifolia, Mucuna pruriens, Piper longum, and Thunbergia grandiflora. Among the ferns, both terrestrial ferns and epiphytes such as Lycopodium clavatum, Dryopteris filix-mas, Gleichenia dichotoma, Lygodium japonicum, Drynaria rigidula, Angiopteris evecta, Asplenium nidus, and Pyrrosia nummularifolia are present (Figure 2a and b).

Figure 2.

(a) Thick evergreen forest within Kaziranga National Park, (b) Buceros bicornis (Hornbills) sitting on the tree within the evergreen forest, (c) Group of Elephas maximus (Asian Elephant) in deciduous forest in Kaziranga National Park, and (d) Rhinoceros unicornis grazing in the periphery near swamp.

The moist deciduous forest occurs as isolated patches within grasslands and next to the evergreen forest. This forest consists of primarily deciduous trees which lose their leaves during the winter season. The major tree taxa are Bombax ceiba, Dillenia indica, Albizia procera, A. lebbek, A. odoratissima, Neolamarckia cadamba, Trewia nudiflora, Careya arborea, Lagerstroemia parviflora, and Semicarpus anacardium. The forest floor is covered by different species of Poaceae, Cyperaceae, Convolvulaceae, and Acanthaceae. The fern allies such as Dryopteris filix-mas, Adiantum caudatum, Blechnum occidentale, Polypodium vulgare, and Drynaria rigidula are the common members in this forest (Figure 2c and d).

The grassland areas are scattered and dominated by tall grasses mainly Erianthus ravennae, Phragmites karka, Arundo donax, Imperata cylindrica, and Saccharum procerum along with short grasses like Hemarthria compressa, Microstegium ciliatum, Cynodon dactylon, and Cenchrus ciliaris. However, some trees and shrubs such as Bombax ceiba, Careya arborea, Dillenia indica, Butea monosperma, and Albizia lebbeck also grow scattered within the grassland (Figure 3a and b).

Figure 3.

(a) Grassland and grazing by Rhinoceros unicornis (b) A view of grassland during winter, (c) A view of openland showing Bubalus arnee (Asian Buffalo) and numbers of migratory birds, and (d) A view of swamp showing numbers of Cervus duvauceli (Swamp Deer) in the center.

The openland areas are also scattered especially near the periphery of the swamp. Tree taxa are almost absent but there are some scattered shrubs such as Melastoma malabathricum, Cassia tora, and Clerodendron viscosum. The openland area is covered with short grasses followed by Cyperaceae, Acanthaceae, Amaranthaceae, Solanaceae, and Convolvulaceae. Cynodon dactylon, Cenchrus ciliaris, Chrysopogon aciculatus, Digitaria ciliaris, and Paspalum conjugatum are the common species in short grass communities (Figure 3c).

The swamp habitat is restricted to generally low-lying areas and covers around 11.8% of the park (Das et al., 2014). It is submerged throughout the whole year but during summer (May-August) the swamp habitat may be expanded due to flooding of river channels resulting from heavy monsoonal rainfall. The major marshy and aquatic taxa include Alpinia allughas, Clinogyne dichotoma, Calamus tenuis, Polygonum orientale, Cyperus rotundus, Sagittaria sagittifolia, Eichhornia crassipes, Potamogeton pectinatus, Nymphaea alba, Euryale ferox, Myriophyllum indicum, Ludwigia sedioides, and Nymphoides indica. Additionally, there are some trees and shrub taxa including Syzygium cumuni, Barringtonia acutangula, Dillenia indica, Bombax ceiba, Osbekia stellata, and Costus speciosus that commonly grow on the periphery of the swamp area (Figure 3d).

With regard to wildlife, KNP is mainly famous for its Rhinoceros unicornis (greater one-horned rhinoceros), but the park is also very rich in other animals and birds. The fauna includes 490 species of birds, 43 species of reptiles and 52 species of mammals (Chowdhury, 2003). Besides rhinoceros, other associated large and medium sized mammalian herbivores include Bubalus arnee, Elephas maximus, Bos gaurus, Sus scrofa, Cervus unicolor, Cervus duvauceli, Axis porcinus, Muntiacus muntjak, Presbytis entellus, Macaca mulatta, Macaca assamensies, and Hylobates hoolock. Birds such as Francolinus gularis, Anser erythropus, Houbaropsis bengalensis, Tringa guttifer, Sterna acuticauda, Ardea insignis, and Pelecanus philippensis are commonly seen in the park.

Materials and methods

Field work

Out of a total of 75 surface soil samples, 15 (E1–E15) were collected from the evergreen forest, 15 (D16–D30) from deciduous forest, 15 (G31–G45) from grassland, 15 (O46–O60) from openland, and 15 (S61–S75) from the swamp. In each vegetation type, the samples were procured at about 50 m intervals.

Laboratory work

The surface soil samples were chemically processed employing the standard acetolysis method (Erdtman, 1953). The soil samples were treated with 10% aqueous KOH solution to deflocculate the pollen and spores from the soil followed by 40% hydrofluoric acid (HF) treatment to dissolve silica content. This was followed acetolysis. The samples were washed 2–3 times with glacial acetic acid and then washed 2–3 times with distilled water and sieved through a 500 µm mesh. Finally, the material was kept in a 50% glycerin solution with a drop of phenol. Totals of 259–335 pollen grains per slide of each sample were counted to make the pollen spectra. The pollen taxa have been categorized into arboreal taxa, non-arboreal taxa, extra-regional taxa (highland taxa coming from the eastern Himalaya), and ferns. Similarly, a total of 225–284 fungal spores per slide were counted from the same pollen slides and were categorized into coprophilous and non-coprophilous fungal spores to make fungal spore spectra. For the precise identification of fossil palynomorphs in the sediments, the reference pollen slides available at Birbal Sahni Institute of Palaeosciences herbarium as well as pollen and fungal spore photographs in the published literature (Basumatary et al., 2017; Basumatary and McDonald, 2017; van Geel et al., 2003) were used. Photodocumentation of palynomorphs was made using Olympus BX-61 microscope with DP-25 digital camera under 40X magnification (Figure 4). The pollen and fungal spore spectra were made using TILIA software (Grimm, 2011) (Figures 5 and 6).

Figure 4.

Palynoassemblages recovered from the surface soil samples from the Kaziranga National Park. Explanation of palynomorphs: (a) Bombax ceiba, (b) Duabanga in cluster, (c) Cinnamomum, (d) Litsea, (e) Terminalia, (f) Lagerstroemia, (g) Barringtonia, (h) Shorea robusta, (i) Schima, (j) Semecarpus, (k). Syzygium, (l) Arecaceae, (m) Albizia, (n) Lantana, (o) Pinus, (p) Rhododendron, (q) Asteroideae, (r) Chinoroideae, (s) Impatiens, (t) Convolvulaceae, (u) Cyperaceae, (v) Poaceae in cluster, (w) Polygonum, (x) Nymphaea, (y) Typha, (z) Monolete, (aa) Trilete, (ab) Sporormiella, (ac) Sordaria, (ad) Meliola, (ae) Tetraploa, and (af) Glomus.

Figure 5.

Comparative pollen spectra in relation to the different vegetation types from Kaziranga National Park.

Figure 6.

Comparative fungal spores spectra in relation to the different vegetation types and herbivores impact from the Kaziranga National Park.

Statistical analysis: Canonical correspondence analysis

Five environmental variables were obtained from the pollen assemblages by calculating the total proportion of five vegetation type indicator assemblages in each site: (1) evergreen indicator assemblage score, (2) deciduous indicator assemblage score, (3) grassland indicator assemblage score, (4) openland indicator assemblage score, and (5) swamp indicator assemblage score (Table 1). These variables provide environmental gradients against which to assess the distribution of fungal NPPs. Pollen of wind-blown extra-regional taxa were excluded from the statistical analyses.

Table 1.

Taxa included in each indicator assemblage score.

Vegetation type	Major taxa included
Evergreen (EV)	Cinnamomum, Duabanga, Litsea, Mesua, Schima, Symplocos, Arecaceae, Dipterocarpaceae, Oleaceae, Impatiens, Piperaceae
Deciduous (DC)	Albizia, Careya, Dillenia, Emblica, Lagerstroemia, Lannea, Bombax, Semicarpus, Sterculia, Terminalia, Convolvulaceae, Cyperaceae, Lamiaceae
Grassland (GL)	Butea, Bauhinia, Dillenia, Bombax, Asteroideae, Chinoriideae, Poaceae
Openland (OL)	Barringtonia, Bombax, Clerodendron, Lantana, Melastoma, Bombax, Justicia, Mimosa, Xanthium, Amaranthaceae, Convolvulaceae, Cyperaceae, Euphorbiaceae, Onagraceae, Solanaceae
Swamp (SW)	Syzigium, Eichhornia, Lemna, Myriophyllum, Nymphoides, Polygonum, Potamogeton, Typha, Nymphaea, Onagraceae

Many fungal NPPs have short dispersal distances, and can therefore be overrepresented in locations near fruitbodies but underrepresented at even a short distance from fruitbodies (Van Asperen et al., 2021; Wilmshurst and McGlone, 2005). A square-root transformation was applied to the fungal NPP percentage data to compensate for this effect (Borcard et al., 2018; Legendre and Legendre, 2012; Paliy and Shankar, 2016).

Canonical correspondence analysis (CCA; Borcard et al., 2018; Ter Braak, 1986) was carried out on the transformed NPP data and the five environmental variables to assess the influence of the five vegetation type assemblages on the distribution of NPPs. Collinearity among the vegetation type assemblages was explored by computing Variance Inflation Factors (VIFs). Based on the results of this, CCA with forward selection of explanatory variables was carried out. Canonical axes were tested for significance by permutation ANOVA. CCA was performed in R (Version 4.0.4, R Development Core Team, 2015) using the package vegan (Oksanen et al., 2017).

Results

The presence and abundance of major pollen taxa, which serve as marker taxa and their ecological significance in KNP are listed in Table 2. Diagrams of the pollen and fungal spore spectra are presented in Figures 5 and 6, respectively.

Table 2.

Characterization of marker pollen taxa recovered from the surface soil samples in relation to the different vegetation and landuse from Kaziranga National Park.

Marker pollen taxa Vegetation type/Ecological significance/Indicator
1. Mesua	Evergreen/High rainfall/Forestland
2. Schima	Evergreen/High rainfall/Forestland
3. Litsea	Evergreen/High rainfall/Forestland
4. Cinnamomum	Evergreen/High rainfall/Forestland
5. Duabanga	Evergreen/High rainfall/Swamp
6. Dipterocarpaceae	Deciduous/High rainfall/Forestland
7. Bombax	Deciduous/Forestland/Openland
8. Syzygium	Deciduous/High rainfall/Forestland
9. Albizia	Deciduous/Forestland
10. Semecarpus	Deciduous/forestland
11. Sterculia	Deciduous/Forestland
12. Lagerstroemia	Deciduous/Riparian/Forestland
13. Barringtonia	Riparian/Swamp/Forestland
14. Careya	Deciduous/Swamp/Forestland
15. Melastoma	Deciduous/Swamp/Openland
16. Dendropthae	Evergreen/Deciduous/High rainfall
17. Impatiens	Riparian/High rainfall/Forestland
18. Poaceae	Perennial herb/Grassland/Openland
19. Cyperaceae	Marshy/Swamp
20. Onagaraceae	Marshy/Aquatic/Swamp
21. Eichhornia	Marshy/Aquatic/Swamp
22. Polygonum	Marshy/Swamp
23. Xanthium	Marshy/Swamp
24. Nymphoides	Aquatic/High rainfall/Swamp
25. Nymphaea	Aquatic/High rainfall/Swamp
26. Potamogeton	Aquatic/High rainfall/Swamp
27. Typha	Aquatic/High rainfall/Swamp
28. Justicia	Perennial herb/Openland
29. Convolvulaceae	Perennial herb/Openland
30. Mimosa	Perennial herb/Openland

Evergreen forest: The surface soil samples (E1-E15) are characterized by the dominance of the major evergreen taxa Mesua, Schima, Arecaceae, Symplocos, and Litsea with values of 1.6–4.9% each followed by deciduous elements at values of 1.0–3.0%. Among non-arboreal taxa, Poaceae is recorded with values of 6.0–8.2% and other herb taxa are also consistently encountered with values of 3.3–3.8% in the pollen assemblages. Extra-regional taxa are consistently present but with low values. Ferns, both monolete and trilete, are encountered with ranges of 4.5–8.0% (Figure 5). The most common coprophilous fungal spores are of the taxa Sporormiella, Saccobolus, and Ascodesmis with values of 0.8–5.6%. Podospora, Sordaria, Arnium, and Cercophora were also encountered at low values. Non-coprophilous fungal spores are consistently represented at the ranges of 0.8–14.1%, with Glomus, Meliola, and Microthyriaceae the most common taxa.

Deciduous forest: The samples from the deciduous forest (D16-D30) are characterized by the dominance of deciduous taxa with the ranges of 0.3–4.7% each, compared with evergreen taxa at values of 0.3–1.6%. Among non-arboreal taxa, Poaceae is dominant and varies from 6.5% to 9.4% and the other associated terrestrial and aquatic herbs are also recorded with values of 0.3–4.6%. Extra-regional taxa are represented with maximum values upto 2.1% in the pollen assemblages. Fern spores are also consistently present with maximum ranges of 4.5% and 5.8% respectively.

The coprophilous fungal spores occur with values from 0.9% to 4.9%. Non-coprophilous fungal spores are dominated by Meliola, Glomus, and Mycrothyriaceae as in the Evergreen forest, with ranges from 0.8% to 15.5%.

Grassland: The surface soil samples (G31-G45) from the grassland habitat are characterized by the dominance of Poaceae with an average value of 30.7%. Other associated terrestrial and aquatic taxa occur with maximum ranges upto 9.7%. Arboreal taxa, both evergreen and deciduous elements, namely Mesua, Bombax, and Careya are regularly encountered at low values. The extra-regional taxa are also consistently recorded with maximum values of 2.6%. The monolete and trilete ferns are represented with ranges of 1.9–5.6% in the pollen assemblages (Figure 5). Coprophilous fungal spores are dominated by Sporormiella. Saccobolus, and Ascodesmis with ranges of 1.0–6.9%, with other coprophilous taxa reaching 6.2%. Among the non-coprophilous fungal spores, Helmithosporium is abundant with values up to 11.5%. Meliola and Glomus are regularly recorded with values of 0.5−11.8%.

Openland: The samples (O46-O60) from the openland located adjacent to the swamp are characterized by the dominance of non-arboreal taxa with an average value of 58.9% compared to arboreal taxa at 27.3%, followed by extra-regional taxa (7.7%) and ferns (6.1%). Among arboreal taxa, both evergreen and deciduous elements are regularly encountered at ranges of 0.3–4.9%. Among non-arboreal taxa Poaceae is dominant with an average value of 19.8% and the other herb taxa are consistently represented by values of 0.3–6.1% in the pollen assemblages. The extra-regional taxa are regularly encountered at the ranges of 0.4–3.2%. The ferns, both monolete and trilete, are recorded by ranges of 2.1–4.3% (Figure 5). The coprophilous fungal spores are much more abundant than in the evergreen and deciduous forest and the grassland. They are dominated by Sporormiella, Saccobolus, and Ascodesmis which are recorded at the values of 1.0–20.0% each. The non-coprophilous fungal spores are less abundant that in the forest and grassland areas, with values of 0.7–8.0%.

Swamp: The mud samples (S61–S75) from the swamp habitat are characterized by the dominance of non-arboreal taxa with an average value of 51.5% over arboreal taxa (30.7%). The ferns and extra-regional taxa are also recorded with average values of 9.2% and 8.6%, respectively. Among arboreal taxa both evergreen and deciduous taxa are consistently encountered at the values of 0.3–3.9%. Among non-arboreal taxa, Poaceae is dominant with an average value of 15.6%. The marshy and aquatic taxa are consistently recorded with ranges of 0.6–4.5%. The extra-regional taxa are consistently encountered at the values of 0.3–2.9%. The fern spores, both monolete and trilete, are represented by values of 3.2–5.8% in the pollen assemblages (Figure 5). Among fungal spores, the coprophilous fungal spores are similarly abundant as in the openland samples, and are dominated by Sporormiella, Saccobolus, and Ascodesmis which are represented in the range of 1.8–19.2% each. The non-coprophilous fungal spores are present at similarly lower ranges as in the openland samples of 0.4–7.8%.

Statistical analysis of NPPs frequencies

VIFs based on an initial CCA indicated significant collinearity was present among the environmental variables. Therefore, CCA with forward selection was carried out. Four environmental variables were selected for inclusion in the CCA: Deciduous forest, Grassland, Openland and Swamp (Figure 7). The environmental variables account for 92.4% (constrained inertia = 0.22728, total inertia = 0.24572) of the variance in the fungal NPP data. The first two CCA axes (eigenvalues: CCA1 = 0.2066, CCA2 = 0.01577) explain 90.4% of the variance. The permutation tests show that both the CCA as a whole (p = 0.001) and each CCA axis (each p = 0.001) are significant and VIFs indicate collinearity among the vegetation type assemblages is low in this analysis. CCA1 is closely related to the openland pollen taxa (positive side) and deciduous pollen taxa (negative side), indicating an inverse relationship between forest pollen taxa and taxa typical of open environments. CCA2 is closely related to grassland pollen taxa on the negative side. Swamp pollen taxa have a positive relationship with both CCA1 and CCA2. Sites located in the different vegetation types cluster closely, with sites from deciduous and evergreen forest fairly well-differentiated in the upper left-hand quarter of the graph and sites in grassland habitats in the lower left-hand quarter of the graph, while sites from openland and swamp areas cluster together in the upper right-hand quarter.

Figure 7.

Canonical correspondence analysis (CCA) of non-pollen palynomorph (NPP) types and environmental variables. NPP types (red) and samples (dark green: evergreen forest; light green: deciduous forest; yellow: grassland; orange: openland; light blue: swamp) are plotted against vegetation type indicator assemblages (blue arrows).

NPPs cluster into four main groups (Figure 7). The coprophilous fungal spores, Ascodesmis, Podospora, Sordaria, Sporormiella, and Saccobolus, covary with the openland gradient. While, also present in relatively high numbers in the other vegetation types, they are most abundant in the openland and swamp habitats. Helminthosporium is the only type that covaries with the grassland gradient, which is unsurprising as this taxon consists mainly of molds that grow on grasses. Fungal NPPs that plot in the center of the graph, such as Alternaria, Arnium, Helicoon, Tetraploa, Valsaria, Type1, and Type2, are not strongly controlled by any of the environmental variables and occur at relatively similar proportions throughout the samples. Some of these represent ubiquitous plant pathogens and decomposers (van Geel et al., 2003). All other fungal NPPs (Bipolaris, Cookeina, Dictyosporium, Glomus, Meliola, Microthyriaceae, Teleutospores) most strongly covary with the forest gradient. This group includes a number of species that grow on woody debris (Cookeina, Dictyosporium), as well as plant pathogens and decomposers, and the mycorrhizal fungus Glomus, which is well-known to form associations with tree roots (van Geel et al., 2003), though it occurs in a wide variety of environments.

Discussion

The modern pollen study of the different vegetation types and areas of different land-use in KNP reveals a good agreement with the extant vegetation. However, some site by site variation has been recorded in the fungal spores in the assemblages. A composite diagram shows the relationship between, the vegetation types and wildlife in KNP based on the abundance of local arboreal and non-arboreal pollen taxa and coprophilous fungal spores in the palynoassemblages (Figure 8). The evergreen forest is characterized by the high abundance of evergreen arboreal pollen taxa (31.3%). The high abundance of deciduous arboreal pollen taxa (32.6%) in the palynoassemblages signifies the deciduous forest. The grassland is characterized by the abundance of Poaceae pollen (30.6%). Similarly, the openland area is characterized by the abundance of both Poaceae (20.6%) and other associated non-arboreal pollen (20.2%). The swamp area is characterized by the high abundance of marshy and aquatic pollen (21.9%) followed by deciduous (20.1%), evergreen (10.6%) and Poaceae (15.6%) pollen. The abundance of the coprophilous fungal spores in the openland (60.7%), swamp (59.3%), and grassland (23.9%) are exhibited in the palynoassemblages which indicates that these sites are highly impacted by the herbivores. The evergreen and deciduous forest can be characterized as moderately impacted sites as indicated by the relatively lower abundance of coprophilous fungal spores with average values of 16.4% and 16.3%, respectively in the palynoassemblages.

Figure 8.

Composite pollen and fungal spore diagram in relation to the different vegetation types from Kaziranga National Park.

The samples taken from the evergreen forest reveals Mesua-Schima-Duabanga-Cinnamomum-Arecaceae-Litsea assemblage, showing a good relationship between the pollen and extant vegetation. The abundance of evergreen taxa, especially Mesua, Duabanga, and Syzygium in the pollen assemblage is significant (maximum value up to 4.9%) and is indicative of high rainfall activity in the region, as these taxa are high rainfall indicators (>2500 mm/y; Barboni and Bonnefille, 2001; Singh et al., 1990). The evergreen forest was evident in the KNP by the presence of Mesua and Duabanga pollen in the rhino dung samples (Basumatary et al., 2017), as these aforesaid taxa are dominant in the evergreen forest of the KNP. The presence of marshy and aquatic taxa, such as Cyperaceae, Polygonum, Nymphoides, and Nymphaea pollen, which could have been transported by wild herbivores and birds, indicate natural perennial water bodies in and around the study area (Basumatary et al., 2017; Ekblom and Gillson, 2010; Stivrins et al., 2019). During the daytime after feeding in the swamp areas these animals move toward the surrounding forests for rest, shelter or to forage in the forest.

Among the fungal spore assemblages, the presence of non-coprophilous fungal spores, Microthyriaceae, Glomus, and Meliola was marked. These taxa are characteristic of dense forest vegetation under warm and humid climatic conditions in response to the high rainfall in the region. Specifically, the abundance of Microthyriaceae, Glomus, and Meliola is considered to be indicative of the presence of dense forest vegetation (Cookson, 1947; Hofmann, 2010; Johnson and Sutton, 2000; Loughlin et al., 2018; Medeanic and Silva, 2010; Musotto et al., 2012, 2017; Selkirk, 1975), and this is reflected in the studied samples from KNP. In the paleoecological literature, Glomus is often seen as an indicator of erosion (Shumilovskikh et al., 2021). However, since this fungus is an endomycorrhiza and often associates with trees, in this case the abundance of its spores is due to its abundance in the forest soil (Kołaczek et al., 2013).

The presence of coprophilous fungal spores was marked in the studied samples and the relatively high percentages are indicative of the presence of wildlife. The coprophilous fungal spores may be limited to specific locations frequented by herbivores so can be considered local in origin since they can only actively disperse a short distance which restricts their presence to near to where sporulation took place (Davis et al., 1977; Ekblom and Gillson, 2010; Malloch and Blackwell, 1992; Parker, 1979; Parker and Williams, 2012; Richardson, 2001; Van Asperen et al., 2021; van Geel et al., 2003, 2008; van Geel and Aptroot, 2006; Wicklow, 1992). The frequency of Sporormiella, Ascodesmis, and Saccobolus was relatively higher in openland and swamp areas as compared to the dense forest. In our study, the moderately high value of coprophilous fungal spores (5.6%) was observed in the palynoassemblage which is quite higher than the 2%, considered as a “background” level (Baker et al., 2016; Davis, 1987; Gill et al., 2013; Raczka et al., 2016). These spores can therefore be inferred to reflect local abundance of the herbivore fauna. The forest area is generally dark, windless, cooler and more humid than outside the forest; conditions that are favorable for fungal growth (Musotto et al., 2017; Promis et al., 2010). Monkeys, gibbons, birds, and other arboreal animals are common, and their excreta regularly falls to the forest floor. The diversity of the fungal remains especially the non-coprophilous fungal spores is high in all samples.

The Salmalia-Dillenia-Lagerstroemia-Semecarpus-Careya pollen assemblage was in agreement with the extant deciduous forest vegetation in KNP. The Dillenia-Terminalia-Careya assemblage is significant as it is characteristic of the preferred habitat of wildlife in the Balpakram valley in the Garo hills of Meghalaya (Basumatary et al., 2014) which coincided with the pollen assemblages in KNP. These plants are utilized as the primary food plants preferred by many herbivorous mammals including elephant and deer species (Devi et al., 2022; Neupane et al., 2019; Odden et al., 2005; Steinheim et al., 2005). The consistent abundance of Bombax pollen in the palynoassemblage which is recorded upto 4.7% was marked in comparison to the other associated arboreal taxa. Bombax is a fire resistant plant (Troth, 1976) which is one of the reasons for its abundance in the palynoassemblage. Forest fires during winter are an important part of the ecology for the wildlife of KNP. Herbivory is an important driver of vegetation structure in the region (Ekblom and Gillson, 2010), so the large herbivores may have played a significant role in shaping the structure of plant communities in the KNP. The coprophilous fungi, Sporormiella, Saccobolus, and Ascodesmis are represented consistently in the studied samples and their abundance closely resembles that in the evergreen forest samples and is also indicative of the presence of wildlife habitation in the deciduous forest. These fungi are also present at relatively higher abundances than in the evergreen forest, indicative of the higher impact of herbivores on the deciduous forest.

The percentages of Poaceae pollen are relatively high in the grassland samples (average 30.7%) and the Salmalia-Dillenia-Emblica-Butea-Careya-Poaceae pollen assemblage was identified as characteristic of this habitat. The presence of some arboreal taxa, especially Mesua, Duabanga, and Symplocos, is significant as these taxa do not usually occur in this vegetation type. Given that these taxa are insect-pollinated, they most likely have been secondarily deposited through animal dung where the herbivores ingested the plant parts elsewhere and were subsequently defecated in and around the grassland areas. The presence of arboreal pollen taxa, both evergreen and deciduous, was recorded from the midden dung of rhinoceros from forested and grassland regions of KNP (Basumatary et al., 2018; Hazarika and Saikia, 2010). The pollen clumping in grasses and Bombax, is marked and indicative of their local origin. The presence of pollen grain clumps is a characteristic feature of entomophilous plants whose pollen disperses shorter distances than wind-dispersed pollen grains (Faegri and Van Der Pijl, 1966; Martin et al., 2009). Since the Kaziranga National Park is enriched with swampy areas, the aquatic vegetation need to be included in the pollen spectra for monitoring the status of water level through pollen records in relation to the monsoonal activities. Moreover, the dung of the megaherbivores like one horn rhino also include aquatic pollen and thus, the modern aquatic pollen preservation could act as a baseline for the coprolite studies for tracing the megafaunal extinction during the Quaternary (Basumatary et al., 2017). The generated pollen data would assist in distinguishing the natural forest vegetation from areas impacted by human activities in the region, based on the fossil marker pollen taxa like Poaceae and Brassicaceae (Basumatary et al., 2018; Tripathi et al., 2021).

Among the fungal spores, coprophilous fungi such as Sporormiella, Saccobolus, Podospora, and Ascodesmis are dominant and represented consistently in the palynoassemblages. Herbivorous animals, especially rhinoceros and elephant, feed and defecate in the grassland, dispersing coprophilous fungal spores with their dung. However, although they are more common than in the forest assemblages, coprophilous fungal spores are less common in the grassland than in the openland and swamps. This may be due to the midden behavior of some of the large mammals, especially the rhinoceros, which tends to defecate in specific areas, so the spores are not distributed uniformly on the landscape. The Sporormiella-Saccobolus-Ascodesmis assemblage was present in the midden dung of rhinoceros from grassland areas (Basumatary and McDonald, 2017) from the KNP. Among the non-coprophilous fungi, Helminthosporium and Alternaria are especially dominant. Both taxa are common pathogens of herbaceous plants, particularly grasses. Other fungal spores such as Glomus, Microthyriaceae, and Tetraploa are also present in lower values in the assemblages. However, grasses have a high resistivity to fungal infection due to their silica content (Hayasaka et al., 2008; Park et al., 2006, 2010) which is the main reason for the low fungal diversity exhibited in the grassland.

The palynological study in the openland area identified some distinguishing features of this habitat within the park, as it is characterized by the Salmalia-Dillenia-Mesua-Barringtonia-Litsea-Melastoma-Poaceae-Mimosa pollen assemblage. Grasses are dominant and recorded a maximum value upto 19.8%. However, the arboreal, marshy, and aquatic taxa, Mesua, Bombax, Lagerstroemia, Syzygium, Onagraceae, and Nymphaea are also consistently present in the pollen assemblages. This reflects the excreted dung of herbivorous animals and birds which incorporated these tree taxa through their ingestion in and around the openland areas. Pollen clumping of Poaceae, Cyperaceae, and Polygonum is very common in the palynoassemblages indicating they originate from local sources (Faegri and Van Der Pijl, 1966; Martin et al., 2009). Among the fungal spores the coprophilous fungal spores Sporormiella-Saccobolus-Ascodesmis are dominant in the assemblage and confirmed that the openland habitat can be considered to function as a corridor for wildlife. The abundance of coprophilous fungal spores in the openland areas suggests a direct link of abundance of wildlife and higher amount of decomposed organic matter derived from dung.

The palynological study of the swamp sediments reveals that the Salmalia-Dillenia-Syzygium-Mesua-Duabanga-Litsea-Melastoma-Poaceae-Mimosa pollen assemblage indicates different types of forest vegetation in and around the swamp area of the national park. The riparian forest taxa, Lagerstroemia, Barringtonia, and Duabanga grow luxuriantly along the periphery of the wetland area. Among non-arboreal taxa, the marshy and aquatic taxa are local in source. The other terrestrial non-arboreal taxa, chiefly Asteroideae, Convolvulaceae, and Mimosa, were deposited in and around the areas by the inwash of rainwater. The presence of Rhododendron pollen (a flood marker taxon; Basumatary et al., 2019) indicates flood activity in the region.

Among the fungal spores the non-coprophilous fungal spores predominate but coprophilous fungal spores, especially Sporormiella, Podospora, and Saccobolus, are still comparatively abundant in comparison to the other studied sites. The preserved fungal spores may have originated from surrounding areas and subsequently transported and deposited through rainwater and slopewash. Furthermore, the swamp serves as a focal point for mammals and birds for their food and especially drinking water. The amount of dung, especially the midden dung of rhinoceros, is large. Water availability is an important factor for the germination and sporulation of coprophilous fungi (Ingold and Marshall, 1962; Kuthubutheen and Webster, 1986a, 1986b), and dung deposited in the swamp can be expected to remain wet longer than in the other vegetation types and thus enhance the potential for germination.

Among the non-coprophilous fungi Tetraploa was more abundant than in the other vegetation types, which reflects its ecology as a saprophytic fungus of Poaceae and Cyperaceae, both of which are major wetland taxa. The abundance of Glomus in the palynoassemblage might be the result of transport directly from the surrounding forest, as Glomus is indicative of soil erosion (Kiage and Liu, 2009; van Geel et al., 2003). The diversity of the coprophilous fungal spores is similar to that of the openland samples with abundant spores of Sporormiella, Saccobolus, and Ascodesmis. This pattern is also seen in the rhinoceros dung midden samples (Basumatary et al., 2017).

The presence of the extra-regional taxa, Pinus, Abies, Picea, and Larix in samples from all vegetation types is significant and indicative of strong wind activity from the higher Himalaya but might also be introduced by migratory Siberian birds (Barua and Sharma, 1999), when they fly through pollen-laden environments. The bird diversity documented in KNP is over 521 species of which more than 200 are residents while the rest are migrants, including local migrants. Pollen may adhere to their body and feathers of migratory species and then subsequently be dislodged during grooming while they are in KNP, especially from species that may overwinter in the park.

Studies of modern analogs based on the pollen and fern spore assemblages have shown it is possible to distinguish agricultural land from the fallow and salt marsh grassland (Graf and Chmura, 2006). The presence of coprophilous fungal spores can aid in distinguishing grazed or manured land use from natural vegetation. Similarly, this study can serve as a guideline to differentiate and distinguish the different vegetation types and the presence and impact of herbivores based on the presence and absence of local arboreal pollen taxa along with coprophilous fungal spores especially Sporormiella, Sodaria, and Ascodesmis in the palynoassemblages. Vegetation structure is mainly controlled by herbivores density (Bell, 1982) in African savannah and the woody cover reduction is directly linked to the concentration of herbivores (Dublin et al., 1990), their presence or absence can be documented by the presence of coprophilus fungal spores in the palynological studies of soil sediments. In order to understand the actual reason of decline and extinction of megaherbivores whether by human activities or due to climate-induced environment change (Wroe et al., 2013) documentation of their presence, either directly by skeletal remains or indirectly via proxy such as coprophilous fungal spores is critical. Other evidence for human impact can be the ability to recognize former cropland whether manured or unmanured based on the representation of local arboreal pollen taxa and coprophilous fungal spores in the palynoassemblages preserved in sediments.

Comparison of pollen spectra with canonical correspondence analysis

The CCA confirms that the five vegetation types present in KNP are significantly different in their taxonomic composition and this is reflected in both the vegetation and pollen assemblages. While the fungal NPP assemblages are relatively similar in overall composition between the different vegetation types, there are some differences in abundance of the taxa recovered reflecting the populations levels of herbivores Coprophilous fungal spores are present in significant numbers in all vegetation types, but the concentration is greater in the openland and swamp areas, where herbivores are more abundant than in the forested areas. The other vegetation types are dominated by mycorrhizal fungi, pathogens and decomposers of the plant species common in these vegetation types.

Interaction between vegetation and herbivores

Demonstrating the strong relationship between pollen types and vegetation in an area provides an opportunity to infer changes in wildlife habitat at both a temporal and spatial scale. Complementing the pollen record is the associated coprophilous fungal spore record which can provide an indication of the presence of herbivore populations utilizing the different vegetation types in these habitats and thus responding to their expansion or reduction over time (Ekblom and Gillson, 2010). Integrating ecological studies of all herbivores in the park and their preferred habitats is critical to integrate with the documentation of the association of pollen and vegetation types to better understand how the vegetation and fauna interact through time (Table 3). Equally important is the documentation of the abundance and types of coprophilous fungal spores associated with each species’ dung (Basumatary et al., 2019, 2021; Basumatary and McDonald, 2017) to provide more refined information on what species of herbivores were present and their association with specific habitats and recognize their heterogenous distribution on the landscape rather than just rough estimates of the increase or decrease in herbivore populations through time.

Table 3.

Association between major mammalian herbivores and vegetation types in Kaziranga National Park.

Mammalian taxon	Evergreen forest	Deciduous forest	Grassland	Open land	Swamp	Reference
Rhinoceros unicornis	++	+++	+++	++	+++	Gurung and Chalise (2015); pers. Comn. Local community
Elephas maximus	+++	+++	+++	+	+++	Neupane et al. (2019); pers. Comn. Local community
Bubalus bubalis	++	+++	+++	+++	+++	pers. Comn. Local community
Bos gaurus	+++	+++	+	++	+++	Imam and Kushwaha (2013); pers. Comn. Local community
Cervus unicolor	++	+++	+++	+++	+++	pers. Comn. Local community
Cervus duvauceli	++	+++	+++	++	++	pers. Comn. Local community
Axis porcinus	+	+++	+++	+++	+++	Biswas (2004), Odden et al. (2005)
Muntiacus muntjak	++	+++	+++	+++	+++	pers. Comn. Local community
Presbytis entellus	+++	+++	+	+	+	pers. Comn. Local community
Macaca mulatta	+++	+++	+	+	+	pers. Comn. Local community
Macaca assamensies	+++	+++	+	+	+	pers. Comn. Local community
Hylobates hoolock	+++	+++	+	+	+	pers. Comn. Local community

: low associated; ++: moderate associated; +++: highly associated.

Conclusions

This study demonstrates that the depositional pattern of pollen and NPP and their relative abundance in different vegetation types in KNP parallels the vegetation present in each type of habit and the impact of herbivores that utilize them. The pollen data from the different vegetation types in KNP reveals a strong relationship with the extant vegetation. In contrast, the depositional pattern of fungal spores varies from site to site due to different levels of wildlife impact and seasonal differences in their presence and utilization of the different vegetation types in the national park. Our study is in close agreement with the vegetation survey and existing forest types in KNP (Champion and Seth, 1968; Das et al., 2014).

As such, the data will be helpful in providing a foundation to differentiate and distinguish the natural forest vegetation from areas impacted by human activities in the region, based on the fossil pollen record given the potential for misidentification of conserved landscapes such as national parks and wildlife sanctuaries and areas that are not set aside or protected and have been heavily impacted by human activity, such as deforestation, farming, and pastoral practices. This may be indicated by the presence and abundance of local arboreal pollen or the relative abundance of coprophilous fungi since unmanured soil has significantly less coprophilous fungi than manured soil (Graf and Chmura, 2006). The openland area is also an important place for wildlife survival as indicated by the presence of marker pollen taxa and the abundance of coprophilous fungal spores. The overall palynological analysis of the swamp sediments could be a reliable and complementary data for the representation of the vegetation types and abundances of herbivores both of which can contribute to paleoecological and paleoherbivory analysis.

Footnotes

Acknowledgements

We thank to Professor Mahesh G. Thakkar, Director of the Birbal Sahni Institute of Palaeosciences, India for laboratory facilities to carry out this research. RG is thankful to Dr. A. A. Mao, Director, Botanical Survey of India for his support. We are very much thankful to handling Editor and anonymous reviewers for their valuable comments and suggestions. First author is also thankful to the forest department, Govt. of Assam for permission to work and necessary help during field visit.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The first author is very much grateful to the Department of Science and Technology, New Delhi for funding (DST No: EEQ-2021/000846 (SERB) the research work.

ORCID iDs

Sadhan K. Basumatary

Eline N. van Asperen

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