Publisher : John Wiley & Sons, Inc Location : Hoboken, NJ, USA ISBN (printPaper-13) : 9781119081104 Title (main) : Savanna Woody Plants and Large Herbivores Copyright (publisher) : © 2019 John Wiley & Sons Ltd Numbering (edition) : I

Creators (editor) : Peter Frank Scogings Professor

Creators (editor) : Dr Mahesh Sankaran

University of Zululand, KwaDlangezwa, South Africa Affiliation : University of Leeds, Leeds, UK

Subject Info : Life Sciences

Title (main) : Herbivores Numbering (main) : II ID (unit) : c7 ID (file) : c7 Event (xmlCreated) : 2019-02-06 (SPi Global) Numbering (main) : 7 Numbering (pageFirst) : 183 Numbering (pageLast) : 212 Object Name (feature) : Box Attribute Value (term) : abbreviation

7

Ecology of Smaller Animals Associated with Savanna Woody Plants

The Value of the Finer Details

Colleen Seymour1,2, Grant Joseph2,3

1 South African National Biodiversity Institute, Claremont, South Africa

2 Percy FitzPatrick Institute of African Ornithology, Department of Biological Sciences, University of Cape Town, Rondebosch, South Africa 3 Centre for Invasion Biology, School of Mathematical and Natural Sciences, University of Venda, Thohoyandou, South Africa

7.1 Introduction

Although savannas are characterized by grass–woody plant coexistence around the world, they have arisen out of different evolutionary histories on the continents, occur on a variety of soil types and are dominated by different phylogenetic groups (Chapter 1). As such, they differ across continents in the characteristics of habitats they provide for small animals (e.g. thorny African acacias, Senegalia, and Vachellia spp., vs North American oaks, Quercus spp.). Phylogenetic differences are associated with differences in plant architecture: for example, trees in Australian savannas are on average 6 m taller for comparable trunk diameter, but their canopy area is only about half that of African counterparts (Moncrieff et al. 2014). Soil nutrients affect resources that woody plants provide for mutualists (e.g. pollinators and seed dispersers) and the defenses used against antagonists (e.g. leaf herbivores). Such differences affect the quality and quantity of resources important to “small” (<25 kg) animals, other than large mammal herbivores, such as nesting sites, food sources (fruit, seeds, nectar, leaves), and the incidence and distribution of chemical and physical defenses among woody plants. Nutrient availability and phylogenetic differences have also meant that woody species respond differently to disturbances such as fire (Chapter 13), which in turn affects resources available to small animals.

Despite the varying habitat characteristics, evolution has seen the small fauna of the world's savannas often having functionally equivalent roles. There has been some degree of functional convergence where niches have been filled by distantly related taxa in some circumstances, but by closely related taxa in others. In this chapter, we consider the numerous small animals that often escape attention, but which may have effects on savanna functioning no less marked than that of large herbivores. We consider the ecological importance of small animals through their interactions with woody plants in their roles as folivores, gall-formers, frugivores, pollinators, granivores, and detritivores. We focus on the interactions of small animals and woody plants based on the resources made available by the plants themselves, with consideration as to how this has shaped the ecology and evolution of savanna systems. Some attention is also given to the effects of climate and land use, and key examples of ecologically and evolutionarily important plant–animal mutualisms. We trace the interactions between woody species and small animals in savannas at different stages of the woody species' lifecycle, which allows comparison of both convergent and divergent evolutionary responses to the different niches furnished by woody plants in savannas on different continents.

7.2 Woody Plant Seed Herbivory

7.2.1 Seed Herbivores

Seed herbivory can affect both fecundity and long-term population persistence of plant species (Russell et al. 2010). Small animals can bring about surprisingly noticeable changes in savanna structure, through seed and seedling herbivory (Weltzin et al. 1997; Vaz Ferreira et al. 2011). Of the small animals, birds, rodents, and invertebrates are important seed herbivores in savannas (e.g. Vaz Ferreira et al. 2011). In Africa, the Middle East, and Central and South America, some of the most important pre-dispersal seed herbivores (predators) are beetles from the subfamily Bruchinae (Chrysomelidae, but formerly in the Bruchidae). These beetles can be responsible for as much as 95% of seed loss (Silander 1978; Rohner and Ward 1999), although usual losses are between 4 and 35% (Coe and Coe 1987). Bruchinae infestation can vary greatly between plants within a population (Traveset 1991; Derbel et al. 2007) and between years (Ernst et al. 1989; Miller 1996a). In Australia, beetles of the genus Dryophilodes (Anobiidae), weevils of the genus Melanterius (Curculionidae) and some chalcid wasps are the primary pre-dispersal invertebrate seed herbivores (Andersen and Lonsdale 1990). Interestingly, most anobiid beetles are woodborers, but it appears as if Dryophilodes radiated to become seed predators along with Eucalyptus and other members of the Myrtaceae that they infest (Andersen and New 1987). Rates of weevil predation of seeds of Australian acacias seem also to be very variable, anywhere between 0.8 and 84.5% (Auld 1986). In North American oak savannas, acorn weevils (Curculio spp.; Udaka and Sinclair 2014) infest seeds, but their relative impact on oak population dynamics and structure seem not to have received much attention (Table 7.1). Bruchinae attack may not be all bad: it may improve seed germination by perforating the tough seed testa and allowing water uptake. Generally, however, Bruchinae attack is detrimental to germination (Ernst et al. 1989). Okello and Young (2000) found just over 20% of Bruchinae- damaged seeds germinated compared with 85% of non-damaged seeds, whereas Martins (2013) found 6% germination in damaged seeds compared with 79% for undamaged seeds in Acacia drepanolobium. Whether or not seeds can germinate after Bruchinae infestation appears to be linked to the timing of germination. If germination is early in the beetle's development, then the cotyledons and radicula may not yet be damaged, and the seeds can still germinate (Coe and Coe 1987; Miller 1994a).

Table 7.1 Summary of interactions between small animals and savanna woody species across continents.

Africa and Middle Central and South Australia East North America America

Woody plant Beetles: genus Beetles from the Beetles from the Beetles from the subfamily seed Dryophilodes (family subfamily Bruchinae family Bruchinae (family herbivory (on Anobiidae), Melanterius (family Chrysomelidae) Curculionidae Chrysomelidae) (Traveset tree) (Curculionidae); some (Ernst et al. 1989; Miller (Udaka and Sinclair 1991) chalcid wasps (Auld 1996a; Rohner and Ward 2014) 1986; Andersen and New 1999; Derbel et al. 2007) 1987; Andersen and Lonsdale 1990)

Woody plant Ants (Orians and Primarily vertebrates Vertebrates: blue jay Vertebrates (Macedo 2002; seed and fruit Milewski 2007); (Coe and Coe 1987; (Cyanocitta Lessa and da Costa 2010), dispersal marsupials (Dennis Middleton and Mason cristata; Johnson often birds (Christianini 2003) 1992; Miller 1994c); dung and Webb 1989), and Oliveira 2010); beetles for secondary woodpeckers secondary dispersal by ants dispersal (Heymons and (Scofield et al. 2011) and dung beetles (Estrada von Lengerken 1929) and squirrels and Coates-Estrada 1991) (Borchert et al. 1989)

Animals that Invertebrates Invertebrates (Seymour Prairie dogs Invertebrates hinder woody 2009), rodents, small (Cynomys plant seedling antelope (Rocques et al. ludovicianus); establishment 2001) invertebrates (McPherson 1993), larger vertebrates, e.g. deer (Ritchie et al. 1998)

Leaves and Invertebrates (Andersen Variety of vertebrates, Vertebrates, e.g. Leaf-cutter ants (Costa et herbivory and Lonsdale 1990), primarily white-tailed deer al. 2008); mammalian possums (e.g. Runcie megaherbivores and (Ritchie et al. 1998) foliovores relatively small 1999) antelope; invertebrate group (Marinho-Filho et al. outbreaks 2002)

Pollination Birds seem to be Variety of insects Wind pollinated Birds (humming birds), and particularly important (particularly bees, flies, bees, flies, moths, wasps, nectarivory (Orians and Milewski butterflies, moths and bats (Oliveira and Gibbs by small 2007), but also insects, wasps) but also birds, 2002) animals e.g. wasps bats (Salewski et al. 2006; Martins and Johnson 2013; Symes and Yoganand 2013) Parasitoids (insects whose larvae develop within, and eventually kill, their hosts) of Bruchinae may help limit the damage the beetles inflict on seeds. The main parasitoids of Bruchinae seem to be chalcid or ichneumonid wasps. These wasps usually parasitize the beetle's eggs or larvae (e.g. Gagnepain and Rasplus 1989). The degree of parasitism is variable. In a study conducted in a Costa Rica savanna, infestation of bruchid beetles by ichneumonid wasps was 90% within trap bags, although for seeds collected from the field, this figure was 30–39% (Traveset 1991). In Botswana, 0–4.7% of Bruchinae larvae had been parasitized (Ernst et al. 1989). Parasitoid infection is likely variable because of different population dynamics of the parasitoids and their hosts: parasitoids often lag their hosts in abundance, following natural increases and decreases in population size (Ives 2009).

Parasitoids do seem to increase seed viability. The wasp Dinarmus magnus parasitizes Bruchidius sp. that infest A. drepanolobium. In a recent study, just over 18% of seeds containing Dinarmus germinated, compared with 6% of seeds containing Bruchinae (Martins 2013). The value of limiting seed-predating beetles by parasitoids requires further research, but may be important for Acacia populations, if they allow sufficient seeds to germinate and ultimately recruit into mature life stages (Martins 2013).

In addition to parasitoids, ants may defend seeds from invertebrate herbivory. Ants have been found to remove Bruchinae eggs from pods in Costa Rica (Traveset 1990a) and Mexico (Pringle 2014), although no beneficial effect of ant presence was found for acacias in Laikipia, Kenya (Palmer and Brody 2007), and it appears that ants patrol leaves more than pods on A. drepanolobium (Martins 2013). In non-savanna environments, ants have been found to protect Quercus acorns against borer beetles (Ito and Higashi 1991), but whether a beneficial ant–oak relationship exists in North American oak savannas appears not to have been investigated.

Birds, mammals, and invertebrates may disperse seeds, benefiting woody species. Some, however, may also consume and damage seeds so that they are no longer viable (Miller 1994b; Weltzin et al. 1997; Linzey and Washok 2000; Barnes 2001; Walters et al. 2005; Pérez et al. 2006). For example, ants have been found to be seed predators in savannas in Texas (Weltzin et al. 1997), Venezuela (Pérez et al. 2006) and Brazil (Vaz Ferreira et al. 2011). Prairie dogs and associated ants in North America control Prosopis populations through seed and seedling consumption (Weltzin et al. 1997). In Australia, granivory is not common among the marsupials (Russell et al. 1993) and the diversity and abundance of small rodents is considerably lower than that of North America; in Australia, ants are far more important in seed predation (Morton 1985). Although rodents and ants can be seed predators, they can also be important seed dispersers (see below).

Ingestion by large mammalian herbivores may reduce the damage by Bruchinae beetles, as the larvae are digested in the mammal's gut (Coe and Coe 1987), reducing the abundance of Bruchinae in the next generation (Miller and Coe 1993). Large herbivorous mammals also remove the seeds from the vicinity of the parent plant, presumably from where invertebrate herbivores are at their greatest densities (Table 7.1). Once consumed and dispersed by mammalian or reptilian herbivores, and excreted in dung, seeds are still prone to predation, and can be secondarily consumed by animals searching in dung. For example, birds, baboons, monkeys, and rodents have been observed to pick seeds from dung (Traveset 1990b; Dudley 1999; Seymour and Milton 2003). Millipedes can feed on the emerging cotyledons of seeds germinating in dung (Seymour and Milton 2003) and certain Bruchinae beetles infest seeds after dispersal in dung (Traveset 1990b).

Woody species have evolved a number of strategies to reduce seed predation. Although the timing and amount of seeds produced are largely constrained by abiotic factors such as rainfall, woody species may also produce large numbers of seeds in synchrony to satiate seed herbivores (Kelly 1994), or they may engage in “predator cleansing” (sensu Kelly and Sork 2002) by aborting fruits early, killing a cohort of seed herbivores in the process, and then flowering immediately afterwards with successful seed set, as has been found in Acacia tortilis in Tanzania (Mduma et al. 2007). Production of large numbers of seeds in some years to reduce seed predation has also been observed in North American savannas (Koenig et al. 1994). Woody plants may also provide extrafloral nectaries (EFNs) or expanded thorns to encourage the presence of ants, but this seems mainly to act against leaf herbivory, although they may also help reduce seed predation of developing seeds by other insects and even large herbivores (see above and Willmer and Stone 1997). 7.3 Woody Plant Seed and Fruit Dispersal

Seed dispersal is important for avoiding competition and mortality near the parent plant, establishment of new metapopulations, and ensuring seed arrival at the most suitable microhabitat (Howe and Smallwood 1982; Child et al. 2010). Seed dispersal by animals is a crucial mutualism. In southern Africa, 60% of woody species are dispersed by animals, primarily vertebrates (Coe and Coe 1987). This figure is estimated at 50–60% for the Cerrado (Macedo 2002) and it seems likely that animal dispersal, particularly by ants (myrmecochory), is important in Australian savannas (Orians and Milewski 2007).

Large ungulates and megaherbivores are important for are key to dispersal in the Paleotropic savannas of Africa and India (Middleton and Mason 1992; Miller 1994c). Lower densities of large ungulates in Neotropical savannas has led to smaller animals assuming an important role in seed dispersalthis role, but it is likely that preceding the Pleistocene defaunation of South America, megafauna were responsible for megafaunal fruit dispersal was instrumental for of certain Neotropical savanna woody species (Guimarães et al. 2008).

Here we focus on the role of small animals and, because theThe scale at which dispersal occurs has direct consequences for plant recruitment, diversity, and spatial patterning (Christianini and Oliveira 2009), here, we evaluate the effects of both long-distance dispersal (e.g. by birds and small mammals) and short-distance, often secondary, dispersal by invertebrates (e.g. ants and dung beetles).

7.3.1 Diplochory

Diplochory is the dispersal of seeds in two or more steps, each step by a different dispersal agent. It emerges that the first and second steps of diplochory achieve different outcomes for the plant (Vander Wall and Longland 2004). The first step allows establishment at far distances from the parent plant, and escape from density-dependent seed and seedling mortality near the parent, whereas the second step ensures that seeds are delivered to suitable microsites for successful seedling establishment (Vander Wall and Longland 2004).

In Neotropical savannas, small animals emerge asare prominent role-players in distance dispersal and woody species metapopulation dynamics, and diplochory involving vertebrates and invertebrates is increasingly recognized (Christianini et al. 2007), particularly involving birds and ants. In a study by Christianini and Oliveira (2010), 32% of the fruit crop was removed from canopies by birds, while 25% of the fruit crop landed beneath the parent plants (some of which had been dropped by birds). Most of the diaspores that had fallen to the ground below the canopy were then removed by a diversity of ant species (representating five genera; Christianini and Oliveira 2010). Birds tended to transport diaspores (i.e. fruits or seeds that act as the unit of plant dispersal) 40 times farther than ants did, but seedlings were only found close to ant nests (Christianini and Oliveira 2010), highlighting the role of ants in facilitating establishment (Table 7.1).

In African savannas, the role of large herbivores in dispersal cannot be overstated. It is noteworthy that dispersal of Acacia spp. (e.g. A. tortilis and A. nilotica), which characterize most African savannas, declines markedly in the absence of large herbivores. The hard, dry pods of these trees remain shaded beneath the parent, increasing predation and competition, and denying the benefits of secondary dispersal by dung beetles, a key mode of dispersal in savannas that are rich in both ungulates and megaherbivores (Miller 1996b). Dung beetles can transfer seeds within fecal matter for up to 15 m (Heymons and von Lengerken 1929). Communities of different species of Scarabaeinae can bury up to 95% of seeds excreted per dung pile (Shepherd and Chapman 1998), providing protection from seed predation. Estrada and Coates-Estrada (1991) found that seeds transported in, and buried with, dung (by Scarabaeinae) were three times more likely to germinate and establish, due to reduced competition, establishment at favorable microsites, and reduced predation.

7.3.1.1 Seed Dispersal by Birds

In North American oak savannas, the blue jay (Cyanocitta cristata) plays an important role in long- distance acorn dispersal and demography (Johnson and Webb 1989). Jays cache acorns underground, and preferentially cache in grassland systems following burns, fostering germination in habitats most suitable for oak establishment (Johnson et al. 1997). Other birds (e.g. woodpeckers; Scofield et al. 2011) are also important seed dispersers in these savannas.

In African savannas, nutrient and clay-rich Macrotermes termite mounds are establishment sites for fleshy- fruited woody species not usually found in the savannas; frugivorous birds visit these mounds frequently, ultimately importing, and increasing establishment of, other fleshy-fruited species on the mounds, which in turn enhances seed dispersal to other mounds (Joseph et al. 2012).

Species of mistletoe, obligate stem parasites, occur across the world. They are usually dispersed by a small set of passerine bird species, and have an extremely sticky viscin that stays on the seed, even during gut passage, so that the seeds end up on twigs after being wiped off the bird's beak or defecated out (Wenny 2001). Mistletoe seeds that land on the ground do not survive (Wenny 2001). Mistletoes rely on only a few bird species because they have highly specific dispersal requirements, needing to be deposited on appropriate host species and twigs. Twig size is important: those with small diameters seem unable to survive if parasitized by mistletoe, so both the mistletoe and host twig die, and thicker twigs often have bark that is too thick for the mistletoe to penetrate (Sargent 1995). Thus, certain bird species make better dispersers of mistletoe than others, because they tend to perch on twigs in the appropriate diameter size classes (Reid 1989).

7.3.1.2 Invertebrate Seed Dispersal

In Australian savannas, invertebrates are the primary agents of woody plant dispersal: fleshy fruits, which are usually vertebrate-dispersed, are uncommon in Australia, relative to other continents. Australia harbors 10% of the world's ant species (Braithwaite1990) and myrmecochory is more prevalent in Australia than on any other continent, as is the occurrence of seed-associated food bodies that attract ants (elaiosomes; Berg 1975). The transportation of seeds with elaiosomes to ant nests ensures that seeds reach nutrient-rich sites (Culver and Beattie 1978) and avoid ground-level predation and competition with the parent plant (Howe and Smallwood 1982).

7.3.2 Fruit Dispersal

The fleshy covering on seeds that eventually led to fleshy fruits initially arose through selection for defense of seeds against invertebrate predation; later it came to facilitate seed dispersal, driving the coevolution of fleshy-fruited species and modern frugivores (Mack 2000). Many mammals (e.g. primates and elephants) are important dispersers of fleshy-fruited species, as are birds. Within the Neotropics, despite a relative paucity of large ungulate herbivores, a multitude of mammals disperse seeds. The maned wolf (Chrysocyon brachyurus) provides an interesting example (Figure 7.1). Solanum lycocarpum, locally called fruta-do-lobo (wolf's fruit), is a woody species common to the Cerrado. Its fruit is an important constituent of wolf dietary intake in the dry season (Aragona and Setz 2001) and recent declines in wolf numbers may ultimately impact on its spatial distribution. Many small marsupials are importantcrucial seed dispersers in South American savannas (e.g. Lessa and da Costa 2010). Alves-Costa and Eterovick (2007) suggest that, in defaunated fragments of the Cerrado, coatis (Nasua nasua, Procyonidae, racoon family) maintain seed dispersal services for many woody species, promoting gene flow within patches of structure, and facilitating regeneration of degraded sites. The coatis play a significant role in germination, too. A 50% increase in germination success for Myrcia guajavaefolia occurred following pulp removal by coatis (Alves-Costa and Eterovick 2007). Figure 7.1 The maned wolf (Chrysocyon brachyurus) of the Cerrado is an important seed disperser through its consumption of fruit. Declines in this species, as well as that of others, like coatis (Nasua spp.), are likely to negatively impact distribution and survival of many Cerrado woody species. Source: Drawing by C. Seymour.

Dispersal of the buriti palm (Mauritia flexuosa) of the sandy north-western Cerrado illustrates the endozoochorous contribution of multiple vertebrate species. In the canopy, three psittacids (parrots), Ara manilata, A. ararauna, and Amazona aestiva, consume 90% of the fruit, dropping much of it, as partially eaten fruit, to the palm's base. Other birds feeding on the fruits include members of the Thraupidae, Icteridae, Falconidae, Corvidae, and Rallidae. Once fruit has been dropped or has fallen, a number of terrestrial birds and mammals feed upon it, including opossums, rodents, and maned wolves (Macedo 2002).

A review of the Gran Chaco of Argentina provides a disconcerting example of how the loss of mammalian frugivores is predicted to impact woody plants. In this savanna, 80% of the largest herbivores are threatened. Given that 50% of Chaco woody plant species are endozoochorous, the demise of these mammals is anticipated to alter woody community composition and, ultimately, savanna vegetation structure (Periago et al. 2015).

7.4 Woody Plant Seedling Establishment

Seedling establishment is a primary limiting factor of woody plant cover in arid savannas (Higgins et al. 2000). Here we explore how an array of invertebrates and small vertebrates influence seedling establishment.

Although there is an arrayare a number of mechanisms and mutualisms for seed dispersal, dispersal to suitable microsites may not be sufficient to ensure successful recruitment of woody species. Mycorrhizae are associated with improved seedling survival and growth rates for many (perhaps most) woody species (Janos 1980; Martins et al. 1996), yet the importance of this mutualism is often not considered (Frank et al. 2009). Successful establishment of woody species often depends on dispersal of both the seed and the mychorrizal symbiont. Although early successional plant species may make mycorrhizae available for later successional species (Högberg and Piearce 1986), rodents may also transport mycorrhizal fungi. In oak savannas, Frank et al. (2009) found that rodents dispersed spores of hypogeous fungi in their fecal pellets for distances up to 35 m from mature trees, considerably further than the 5-m root zone, the other source of fungal inoculum. Loss of rodents could therefore have consequences for savanna woody plant establishment and woody species community composition, as has been postulated for forest systems (Kiers et al. 2000; Gehring et al. 2002). Although rodents may facilitate woody species establishment through dispersal of mycorrhizae, they, along with lagomorphs and invertebrates, also emerge as major predators of seedlings (Griffin 1976; Weltzin et al. 1997; Shaw et al. 2002; Goheen et al. 2004). The relative importance of each of these groups may vary with annual rainfall, with insects being more important predators during low rainfall years, when rodent numbers are lower.

The interconnected nature of ecosystems means that there are a number of interactions between larger herbivores and smaller species. For example, rodent densities and invertebrate communities change in response to the presence and density of large herbivores, affecting survival rates of seedlings of woody species and, ultimately, savanna vegetation structure (Shaw et al. 2002; Goheen et al. 2004, Chapter 18). In a study on A. drepanolobium in Kenya, in plots from which a variety of large mammals, including elephant (Loxodonta africana), giraffe (Giraffa camelopardalis), African buffalo (Syncerus caffer), eland (Taurotragus oryx), and a variety of others had been excluded, the rate of seedling damage was greater than in plots from which large mammals had not been excluded, suggesting a compensatory response to reduced competition by rodents and invertebrates (Shaw et al. 2002). Damage to seedlings in plots to which only invertebrates had access was no different to those at which both rodents and invertebrates had access, suggesting that invertebrates were responsible for most of the damage (Shaw et al. 2002). Similarly, although large herbivores increased the chances of seedlings dying from desiccation indirectly through removal of grass cover, their presence was associated with lower numbers of rodents and invertebrates, which ultimately translated into higher survival of seedlings (Goheen et al. 2004). Some rodents include grass (which competes with woody seedlings) and invertebrates (some of which may feed on woody plant seedlings) in their diets, however, so the interaction between rodent numbers and woody plant recruitment is not straightforward (Bergstrom 2013).

Once seedlings have progressed beyond the cotyledon stage, spines may retard herbivory by small mammals (Cooper and Ginnett 1998). Small browsers (e.g. steenbok, Raphicerus campestris, and dik-dik, Madoqua spp.) can still have a marked effect on woody seedling growth. In Kenya, small mammal browsing was associated with a sixfold reduction in the rate at which seedlings <0.5 m in height recruited to the next size class, which, when combined with low rates of plant mortality in larger size classes, equated to an almost zero change in woody plant density (Augustine and McNaughton 2004; Sankaran et al. 2013).

7.5 Leaves and Herbivory

In African, Asian, and North American savannas, large herbivores fill much of the browsing niche, but in the savannas of Australia and South America, smaller animals dominate the folivory niche (Table 7.1).

Invertebrates can be significant consumers of leaves across the savannas of the world and damage can range from defoliation of entire populations to, more commonly, defoliation of scattered individuals (Andersen and Lonsdale 1990). Outbreaks of herbivorous insects, resulting in severe defoliation, can make fast-growing plant species more resistant to invertebrate attack in the following year, but may have the opposite effect in slow- growing plant species (Bryant et al. 1991). Heavy defoliation has been found to be associated with reduced seed set in the following year in both fast- and slow-growing species (Rockwood 1973).

Leaf-cutter ants (Atta and Acromyrmex spp.) in South, Central, and southern North America, can be key consumers of woody species. Atta species in the Cerrado have been estimated to consume between 1.3 and 3.7 times the amount of woody plant biomass of all other invertebrates combined, comparable with about a quarter of that consumed by all grazing and browsing mammalian herbivores in the Serengeti (Costa et al. 2008). Plants have evolved a mutualism to reduce herbivory: those plants with symbiotic endophytic fungi in their cells are less likely to be consumed by leaf-cutter ants (Estrada et al. 2013). Endophyte loads in leaves negatively affect growth of incipient leaf-cutter colonies, the time at which the colonies are most prone to mortality (van Bael et al. 2012). Leaf-cutters and fire may have interactive effects on Neotropical savanna structure; damage by leaf-cutters and other herbivores is greater on burned than unburned plants (Lopes and Vasconcelos 2011). Ant foraging on plants is promoted by sources of liquid food, that is, EFNs, provided by the plant itself, honey dew from phloem-feeding hemipterans and exudates from lepidopteran larvae (Oliveira and Freitas 2004, and references therein). The diets of ants are wide and can include both plant and animal exudates along with animal prey, so the effect of a large number of foraging ants on plants can be positive or negative, and marked, given their great abundance (Oliveira et al. 2002). If ants tend herbivorous insects, their effects on the host plant will be negative. If they aggressively defend the plant from herbivores, then their effect will be positive (Oliveira and Freitas 2004). Surveys in the Cerrado found that 15–25% of woody species possess EFNs, accounting for between 7.6 and 31.2% of individuals surveyed (Oliveira and Freitas 2004). Qualea multiflora individuals that had no ants had 1.6 times more herbivores attacking leaves than ones with ants (Del-Claro et al. 1996). Australia is known to be rich in ant species (Braithwaite 1990). Ant species richness in the Cerrado is also high and could be partly explained by the variety of woody species offering EFNs, which could point to some ant–plant specialization (Ribas et al. 2003).

There is a high degree of host specialization among phytophagous insects, mainly because specialization is needed to overcome plant chemical and physical defenses. Related insect species tend to use plants that are chemically similar, even if taxonomically unrelated (Ehrlich and Murphy 1988; Jaenike 1990). Lycaenid butterflies often engage in mutualistic interactions with ants (e.g. caterpillars provide sugar-rich solutions for ants in exchange for protection). This mutualism seems to allow these butterflies to survive on sub-optimal host plant species and may allow butterflies to shift or expand their host range (Forister et al. 2011).

In African savannas, ants have been found to defend trees from mammalian herbivores. The benefits extend beyond protection from mammalian herbivores, however. In a striking example of ecological cascades, large mammal exclusion over a decade saw A. drepanolobium reduce investment in food and nesting resources for mutualist ant species. The reduction in resources sawwas associated with changes in species composition of the ant community away from a species highly reliant on the resources, but also highly protective (Crematogaster mimosae). This in turn led to greater damage and mortality by woodborer (cerambycid) beetles (Palmer et al. 2008). Reduced provision of EFNs also saw C. mimosae tending damaging hemipterans to a greater degree (Palmer et al. 2008). Incidentally, patrolling ants seem able to deter elephant herbivory to an extent that can be detected at the landscape scale, altering woody cover (Goheen and Palmer 2010). Ant–plant mutualisms are costly to trees (Palmer and Brody 2013), but it seems that these mutualisms are important defenses against sporadic bouts of deleterious elephant herbivory (Stanton and Palmer 2011). In the Cerrado, ants have been found to reduce invertebrate herbivory (Oliveira et al. 1987; Del-Claro 2004; Lange et al. 2013; Lange and Del- Claro 2014), as have wasps (Alves-Silva et al. 2013). As African savannas undergo conversion to cropland at an unprecedented rate, there is concern that ant species responsible for important ecosystem services may be lost from invertebrate assemblages. For example, a recent study in southern Africa has shown that cropland harbored less than half the ant indicator species of the near-pristine savanna system, and that many missing species were responsible for a broad range of services that included not only control of invertebrate herbivore numbers, but also pollination, soil mixing, and nutrient cycling (Mauda et al. 2018).

Gall-forming insects also represent a form of herbivory, changing plant architecture and resources. Gall- formers are particularly diverse in the Cerrado (Lara and Fernandes 1996). Interestingly, unlike free-living insects, gall-formers in South America become more diverse with increasing aridity (Fernandes and Price 1988) and with declining soil fertility (Gonçalves-Alvim and Fernandes 2001). This unanticipated outcome probably arises because plants that live in stressful environments often have sclerophyllous leaves (as in the Cerrado). Sclerophyllous leaves are usually long-lived and tough, and therefore tend to have a low chance of abcission (Price et al. 1998). These tough leaves likely also protect galling insects from predators and parasites (Gonçalves-Alvim and Fernandes 2001). The patterns in gall-forming insect diversity with aridity do not hold in Australia (Blanche 2000) or South Africa (Veldtman and McGeoch 2003), however. Instead, it appears that galling insects preferentially choose species with traits that can be manipulated by the galling insect, such as mechanical strength, chemical toxicity, longevity, and woodiness (Veldtman and McGeoch 2003). Future meta-analyses should facilitate identification of environmental and evolutionary factors that drive the diversity of gall-forming insects.

Linked to the high incidence of insect galls in the Cerrado is the occurrence of ant nests in the foliage, which the ant colonies occupy after the galling insect has emerged (Araújo et al. 1995). Given that ants patrol plants and carry costs and benefits, this relationship between galling insects and ants could be a ripe field for further research.

Apart from the obvious effects of climate change on weather and fire regimes, elevated atmospheric carbon dioxide can also affect plant chemistry. Increased CO2 in the atmosphere is likely to be associated with decreased nitrogen concentration in leaves (Curtis and Wang 1998). Higher carbon:nitrogen ratios could be associated with an increase in leaf consumption to meet the nitrogen deficit (Lincoln et al. 1986), but could also be associated with reduced growth rates of insect larvae (Wang et al. 2009). Reduced growth rates might be offset by increased temperatures, which allow faster invertebrate growth (Zvereva and Kozlov 2006). However, the effects of elevated CO2 concentrations seem not to affect nitrogen-fixing plant species, so insect species feeding on these do not exhibit reduced growth rates (Karowe and Migliaccio 2011). Over time, the advantage to invertebrates feeding on leguminous plants over those feeding on non-leguminous plants could translate into changes in invertebrate and plant community composition, with concomitant changes in the ecological processes in which they participate.

7.6 Pollination and Nectarivory

Pollen vectors in most savannas worldwide are small animals, and the vast majority of plant species in the world are animal pollinated, with 78 and 94% being animal pollinated in temperate and tropical communities, respectively (Ollerton et al. 2011). North American savannas are an exception: the dominant Quercus spp. are wind pollinated (Table 7.1).

Insect pollinators are the largest group of animal pollinators, but bats, birds, and even non-flying mammals can also be important pollinators in savannas. For example, in Australian savannas, both vertebrates and invertebrates are important for eucalypt pollination; in particular, Eucalyptus miniata and E. tetrodonta produce high energy yields of nectar, and birds appear to be key pollinators for these two species (Franklin 1994). Nectarivorous birds represent a high proportion of bird species in Australia, and this may be because Australian landscapes are nutrient-poor, so plant species allocate large amounts of energy to carbon-rich exudates, such as nectar (Orians and Milewski 2007). In African savannas, ornithophilous flowers can be a source of forage for far more species than simply specialist nectarivorous birds: Schotia brachypetala (locally called “weeping boerbean” because of the abundant nectar it produces) has been recorded to be visited by 54 bird species, as well as tree squirrels (Paraxerus cepapi; Symes and Yoganand 2013).

Just as birds other than specialist nectarivores may forage from flowers, specialist nectarivores also rely on non-ornithophilous plants to sustain them, for example, only half the plant species visited by humming birds (Trochilidae) in the Cerrado had traits expected for classic ornithophily (Araújo et al. 2013). These non- ornithophilous species thus support humming birds, which indirectly support pollination of the ornithophilous species, because humming birds do not move away to other patches to forage (Maruyama et al. 2013). In African savannas, sunbirds (Nectariniidae) have been observed visiting the flowers of various Acacia(Vachellia and Senegalia) species (Stone et al. 2003). Nectar can be a food source for migrating birds, and woody species such as Balanites aegyptiaca, Maerua crassifolia, Capparis decidua, Acacia raddiana, and Ziziphus mauritiana have been recorded as foraging sites for a number of bird species (Salewski et al. 2006). Of course, it is not just nectar that animals seek, and often the entire flower is consumed by animals, for example, birds (Seymour, pers. obs.), although there is scant mention in the literature of flower consumption in savannas.

One of the most iconic African tree species, the baobab (Adansonia digitata), with its large, showy flowers, has long been known to be bat pollinated (Baum 1995). Bats pollinate other unusual and iconic trees, such as the “sausage tree” (Kigelia africana), although the flowers have also been seen to be visited by various sunbirds, insects, and even monkeys (www.plantzafrica.com/plantklm/kigeliaafric.htm).

Insect pollinators (e.g. bees, butterflies, beetles, and wasps) are the largest group of animal pollinators. Their relationships with woody plants in savannas vary from specialist to generalist. Fig wasps (Agaonidae) are an extreme example of specialized pollinators. Figs (Ficus spp.; Moraceae) occur across the world in many habitats, including savannas (e.g. African savannas; van Noort and Compton 1998), and display a tightly coevolved relationship with their pollinators. With few exceptions, each fig species has a single species of wasp that pollinates it. Small green fruits are entered through a pore by minute female wasps carrying pollen from their own parent plant (Janzen 1979). Once inside the monoecious fruit, a wasp will pollinate hundreds of florets, each with a single ovule, and also lay an egg in each of many of the ovaries. Other pollinating wasps may or may not arrive. The wasp larvae consume the developing seed and remain inside the seed coat, so that ultimately, the plant sacrifices many of its offspring for the opportunity of outcrossing. After about a month, wingless wasps emerge and mate with other wasps that have also just emerged (often their siblings). The females are winged and carry pollen from the newly dehisced anthers to another conspecific fig, for the cycle to resume (Janzen 1979).

Although specialist figs pay a price for specialist pollination, generalist-pollinated species face different challenges. Generalist pollinators, by definition, visit a number of plant species, so some proportion of pollen deposited on stigmas is likely to be heterospecific, reducing the chance of pollen of the right species reaching the ovule, as the stigma becomes blocked by pollen from other species. This is costly to both pollen donor and pollen receiver. A number of mechanisms have evolved to minimize these negative interactions between coexisting species. Among sympatric African acacias, a combination of spatial separation of species (dictated by edaphic factors), temporal separation of flowering seasons between species, differences in flower visitor assemblages (driven primarily by different nectar quantities), and daily temporal partitioning of pollen release reduce deposition of heterospecific pollen (Stone et al. 1998).

Bees are the main visitors to African acacias (Stone et al. 2003). Honey bees (Apis mellifera) can be particularly important pollinators, but they have been observed to collect different resources from different species: nectar from Acacia (Senegalia) senegal and pollen from A. (Vachellia) tortilis, while almost entirely ignoring A. (Vachellia) nilotica and A. (Vachellia) drepanolobium (Stone et al. 1998, 2003). Instead, megachilid bees and syrphid flies were important flower visitors to A. nilotica and A. drepanolobium (Stone et al. 1998). Butterflies are obligate nectar feeders, and so are only observed on African acacias that secrete nectar. Beetles, which can pollinate, but are often also flower predators, are also frequently observed on Acacia flowers (Stone et al. 2003).

In the Cerrado, bees are the chief pollinators of woody species, although one of the most widespread species, Qualea grandiflora, is pollinated by hawk moths (Sphingidae; Oliveira and Gibbs 2002). In fact, hawk moths are responsible for pollination of about 20% of the most common and widespread woody species in the Cerrado (Oliveira et al. 2004). The evidence to date suggests that butterflies are unimportant in Cerrado woody species pollination (Oliveira and Gibbs 2000).

Although ants are useful deterrents of both mammalian and invertebrate herbivores, their aggressive behaviour can deter pollinators. A study of Crematogaster ants on Acacia (Vachellia) zanzibarica found that ants patrolled flowers before and after the flowers were available for pollination, but avoided flowers at the crucial time for pollination, allowing visitation by flying pollinators; it was also found that plants that were patrolled had greater seed set (Willmer and Stone 1997). Young flowers appear to produce a volatile chemical signal, perhaps from the pollen itself, which deters the ants (Willmer and Stone 1997). Once pollination has occurred, it is then in the plant's interest to have the ants patrolling again. Similar findings have emerged from the Cerrado: ants visiting Qualea spp. have been shown to increase fruit set (1.7 times more fruit per bud produced on plants to which ants had access) (Del-Claro et al. 1996).

Although comprehensive studies have considered pollination of woody species in the Cerrado (Oliveira and Gibbs 2000, 2002), pollination in other savannas has received less attention. Further studies on pollination could identify interesting direct and indirect interactions, as seen with ants on acacias in African savannas (Willmer and Stone 1997).

7.7 Nutrient Cycling

Savanna ecosystem productivity depends on both the level of nutrients stored in soils, litter, vegetation and animal biomass, and how such nutrients are transferred between these pools. Nutrient cycling is influenced by a number of factors including fire, climate, and soil microorganisms (generally bacteria and fungi) important to the mineralization process. It is well established that nutrient cycling is important in spatial configuration of savanna woody assemblages (Joseph et al. 2012), in turn influencing a number of animal species associated with this component. Tropical savannas differ from temperate biomes, where invertebrates contribute far less to decomposition of organic matter relative to soil microbes (Seastedt 1984). Although tropical savannas house many invertebrate detritivores, such as earthworms and woodborers, here we consider the significant impacts of termites in savannas of Africa and Australia, and leaf-cutter ants in Neotropical savannas. These two invertebrate groups are key in transforming nutrients held in plant litter that would be otherwise unavailable to woody plants (Holt and Coventry 1990).

Among arthropods in Africa and Australia, termites are arguably the most successful primary decomposers. Two Australian mound-building termite species, Amitermes laurensis and Nasutitermes longipennis, alone mineralized around 10% of annual carbon turnover in a study near Townsville, and if other termite species were included, the likely mineralization by termites would approach 20% (Holt and Coventry 1990). Termite assemblages differ in Australia and Africa. Principal Australian harvester termites include Tumulitermes spp. and Drepanotermes spp., while both Hodotermitidae and the fungus-cultivating Macrotermitinae are absent from Australia. Despite these differences, termite biomass of African and Australian savannas, and by extrapolation, their importance in nutrient cycling, is broadly similar (Holt and Coventry 1990).

The direct foraging of termites in African savannas, together with secondary effects of this foraging, impacts on savanna woody community structure, composition, and spatial arrangement, ensuring a disproportionate impact upon nutrient cycling. This effect has been well described for the Miombo system, Africa's largest savanna woodland. It is an expansive area of 2.7 million km2, characterized by Macrotermes (Isoptera) termitaria set within a matrix of dystrophic soils (Huntley 1982). Macrotermes build epigeal nests containing a subterranean fungus comb cavity. These mounds form prominent features of both African and Indo-Malayan savannas, and can stand 9 m high and 30 m in diameter (Lee and Wood 1971), occupying up to 5% of land surface area (Holdo and McDowell 2004). Macrotermes feed by consuming dry litter, herbivore feces, and dead wood, but also feed on Termitomyces fungus combs (Hinze et al. 2002) to which they feed their feces. These fungi break down lignin, facilitating availability of cellulose (Hyodo et al. 2000).

As a consequence of foraging activity, mound soils concentrate nitrogen, phosphorus, potassium, bases, and micronutrients, and elevate clay content (Seymour et al. 2014). Mounds themselves act as refugia for plants to escape from fire, and have altered hydrology and drainage (Hesse 1955; Dangerfield et al. 1998; Joseph et al. 2013), stimulating growth, diversity, and composition of woody species (Fanshawe 1968). Joseph et al. (2012) showed that as mound size increased in area as a consequence of termite foraging activities, nutrient concentrations in mound substrate increased. As a result, wWoody species in plant families characteristic of the Miombo savanna (Caesalpinioideae, Rubiaceae, and Combretaceae) were found less frequenty on gradually disappeared from these enriched patches and were replaced at area-related and nutrient-dependent intervals by an entirely novel assemblage of woody species adapted to enriched soils (e.g. fleshy-fruited species of families such as Ebenaceae, Capparaceae, Anacardiaceae, Boraginaceae, Rhamnaceae, Sapotaceae, and Solanaceae). These species are often evergreen (in a deciduous-dominated savanna), and many represent riparian assemblages of quite different functional groups (Joseph et al. 2014, 2015).

The resource dynamics of these patches (large termitaria) impact soil and plant resources, as well as disturbances such as fire and herbivory. At the outset, termite foraging establishes a small, but enlarging, nutrient-rich patch. Animals are drawn to these fertile, shaded islands, which transform to hotspots for herbivores (Loveridge and Moe 2004) and small mammals (Fleming and Loveridge 2003). Their defecation adds nutrients. Fleshy-fruited woody species from earlier avian visitors attract more frugivorous birds, depositing further propagules from distant woody species (Figure 7.2). Once mature assemblages establish, dispersal to neighbors speeds the process. Ultimately, woody assemblages emerge that differ functionally (Joseph et al. 2014), geographically, structurally, and taxonomically from the surrounding dystrophic matrix. The additional structure afforded by tall trees can, in turn, facilitate additional roosting and perching opportunities for certain bird guilds, further entrenching the cycle (Joseph et al. 2011). The importance of structure to birds in savannas is emphasized by a study revealing how surrogating woody structure through artificial means can act as a conduit for invasion to systems beyond savannas, with deleterious impacts to biodiversity (Joseph et al. 2017; Box 7.1).

Figure 7.2 The southern yellow-billed hornbill (Tockus leucomelas) and many other frugivorous bird species in southern African savannas play vital roles in seed dispersal. Many of these species are cavity nesters, however, and require large trees in which to nest (Joseph et al. 2011). Source: Drawing by C. Seymour.

Box Box 7.1 Crow Invasion from Savanna to Semi-Arid Shrubland via Anthropogenic Structures as Surrogates for Trees

The pied crow (Corvus albus) is presently invading the south-western aspects of South Africa from savanna systems to the north. Increased crow abundance places additional predation pressure on mammals, reptiles, birds, and insects in the surrounding scrub-vegetation. Recent research conducted in Botswana, Zimbabwe, and South Africa show that transmission line poles contribute to the problem, filling the role of trees and providing nest sites in an environment that would otherwise have offered few nesting and perching opportunities. This is only part of the story: faster vehicles on better roads in South Africa provide more roadkill, building in turn a “reservoir” of well-fed crows, which demonstrates how socioeconomic development can contribute to the unanticipated spread of opportunist species (Joseph et al. 2017). Roadkill per number of people transported was greatest in South Africa, where for each roadkill seen per 10 km stretch, the mean number of people seen being transported was 4.5, compared with Zimbabwe, where the number of people being transported per roadkill was 433. Some noise has been added to the plot to facilitate visualization.

Sizeplot (the area within each circle indicates number of data points for a given value) showing crows 10 km−1 against roadkill count 10 km−1.

Given the importance of functional diversity for ecosystem processes, and that mounds act as refuges for woody plant functional diversity, even as browsing negatively impacts it (Joseph et al. 2015; Seymour et al. 2016), the impact of Macrotermes nutrient cycling is far reaching.With climate change, the need for plant cover on termite mounds may be increasing, to enable maintenance of internal mound temperatures (Joseph et al. 2016; 2018).

Within Neotropical savannas, although the activity of nest-building termites can enhance establishment of woody species (de Oliveira-Filho 1992; Ponce and da Cunha 1993), their impact on nutrient cycling is eclipsed by leaf-cutter ants (in particular, Atta spp.), which emerge as the dominant herbivore in the Cerrado, filling the niche of large herbivores that characterize African savannas (Costa et al. 2008). Interestingly, Atta species also attend to fungus gardens. Wirth et al. (2003) found a 26-fold elevation in nitrogen levels at Atta colombica refuse sites compared with surrounding litter, an effect due not only to foraging activity. Symbiotic nitrogen-fixing bacteria within Atta fungus gardens harnessed additional nitrogen, with each colony fixing up to 1.8 kg nitrogen annually (Pinto-Tomás et al. 2009). The consequent nutrient enrichment by leaf-cutter colonies improves root production and can enhance woody plant diversity at Atta refuse dumps (Farji Brener and Silva 1995; Garrettson et al. 1998). In the Chaco of Argentina and Paraguay, trees preferentially establish on abandoned Atta nest sites, fostering islands of structure (Bucher 1982). In the Neotropical savannas and forests, Atta spp. are pivotal for cycling nutrients from foliage to deeper soils, thus enhancing soil fertility, with direct impacts upon woody community structure and ecological processes (Perfecto and Vandermeer 1993; Farji Brener and Silva 1995).

Over the past decade there has been a growing call from the scientific community for the rapid adoption of technologies and legislation that reduce greenhouse emissions and sequester carbon, following predictions that mid-range climate change scenarios are likely to result in around a quarter of species becoming extinct by 2050 (Thomas et al. 2004). Given this distressing scenario, recent research has revealed that termite mounds, in establishing nutrient-rich islands that serve as refugia and act as foci for revegetation, harbor sub-canopy temperatures far lower than in the surrounding savanna. The effect is particularly marked at warmer extremes and can increase a savanna's ability to withstand aridity, enhance recovery from drought, and potentially stabilize savanna ecosystems in the context of global change (Bonachela et al. 2015; Joseph et al. 2016).

7.8 Conclusions

As savannas change with defaunation, habitat fragmentation, and conversion, and climate change, how might small animals and the functions they perform be affected? The fauna of the world's savannas differ considerably. Whereas African savannas still (in part, at least) house megaherbivores and ungulates, the role of herbivory in South American and Australian savannas is largely filled by invertebrates (Andersen and Lonsdale 1990; Costa et al. 2008, 2016). Similarly, seed predation, dispersal, and pollination of woody species are often also carried out by quite different groups across the continents. It is likely, then, that global change will affect each system in quite different ways.

We have already alluded to the expected devastating effects of defaunation in the Chaco, where almost 50% of large frugivorous mammals, crucial as seed dispersers of over half of the woody species, are threatened and declining (Periago et al. 2015). Large-bodied animals are more likely to undergo declines in response to global change than small-bodied ones (Cardillo et al. 2005), so we may well expect to see more changes in savannas that still hold larger-bodied fauna. The interconnected nature of the biotic and abiotic elements of ecosystems makes the consequences of these losses neither straightforward nor easily predictable.

A number of studies have demonstrated the importance of indirect effects quite elegantly (see Chapter 18). For example, we now know that as megaherbivores are removed, invertebrates and rodents increase, probably because of reduced competition (Ogada et al. 2008; Keesing and Young 2014). Rodents not only change woody vegetation structure by feeding on seeds (Keesing 2000) and seedlings (Shaw et al. 2002), but they can also be associated with increased densities of other fauna as diverse as snakes and fleas (Keesing and Young 2014). These increases, in turn, will likely have a number of consequences for the ecosystem, through various mechanisms such as predation, parasitism, disease transmission, competition, and apparent competition. Interestingly, the presence of rodents affects which part of the plant life cycle might be negatively impacted by wild herbivores (MacLean et al. 2011). When rodents are excluded, wild ungulates impact most on woody plant reproduction; when rodents are present, the impact of ungulates is on plant survival (MacLean et al. 2011).

In another study, removal of megaherbivores saw acacias ceasing to provide resources for arboreal ant communities, which led to a change in the ant community composition away from mutualist species that defend the plants from stem-boring beetles (Cerambycidae), such that those that no longer had the mutualist had double the mortality of those with the mutualist (Palmer et al. 2008). Mutualist species also changed their behavior and began farming sap-sucking hemiptera (Palmer et al. 2008).

With global change, not only are megaherbivores being lost, but other wild herbivores are being rapidly replaced by domestic herbivores, with a myriad of effects on plant and animal communities in these systems (du Toit and Cumming 1999). These effects include changes in plant and animal species (Goheen et al. 2010) and functional (Joseph et al. 2015) composition. Replacement of a mixture of different herbivore feeding guilds by grazers alone facilitates tree seedling recruitment, usually because grazers remove grass, which normally competes with woody seedlings (Goheen et al. 2010; Rocques et al. 2001; O'Connor et al. 2014), contributing to woody encroachment.

Woody encroachment, the phenomenon in which woody cover increases at the expense of grassy cover, is a global problem (Burrows et al. 1990; Archer et al. 1995; van Auken 2000; O'Connor et al. 2014). Although a recent review (Eldridge et al. 2011) concluded that woody encroachment need not necessarily have negative impacts for ecosystem functioning, various studies have found negative consequences for small mammals (Blaum et al. 2006, 2007), reptiles (Meik et al. 2002), birds (Seymour et al. 2015) and invertebrates (Blaum et al. 2009). Increased woody structure negatively impacted dung beetles, reducing species diversity and body size (Steenkamp and Chown 1996). All of these changes in species communities, and the functional groups represented within them, are expected to have implications for various ecosystem functions and services. For example, dung beetles are not only important for dung removal, seed dispersal, and nutrient cycling, but they are also key in the control of pest flies and internal parasites (Bornemissza 1970; Nichols et al. 2008; Nichols and Gomez 2014). How severe changes to these functions might be remains to be investigated.

Woody encroachment has also been facilitated by suppression of fire and increased concentrations of atmospheric CO2, associated with anthropogenic climate change (see O'Connor et al. 2014, for a review). Changes to the fire regime have implications for various small animal taxa, with changes seen in ant (Andersen 1991; Parr et al. 2004, but see Vasconcelos et al. 2008), other invertebrate (Andersen and Müller 2000), rodent (Beck and Vogl 1972; Vieira 1999) and bird (O'Reilly et al. 2006) community composition. Fire also interacts with small rodents to have different effects on savanna structure (e.g. Chidumayo 2013). Again, these shifts are likely to be associated with changes in representation of functional groups among these taxa, and testing whether these changes indeed translate into changes in ecosystem function is a ripe new field for research.

Climate change and associated increases in atmospheric CO2 concentrations are likely to change savanna structure through changes in rainfall, temperature, and the frequency and severity of climatic events such as drought (IPCC 2013). Elevated CO2 favors woody plants over C4 grasses, changing savanna structure (Bond and Midgley 2012), with concomitant effects for small fauna. In addition, elevated CO2 should see decreased nitrogen investment in leaves (Curtis and Wang 1998), which could have a number of implications for insect larvae that feed on these, and the animals that prey on the larvae, and changes in functional group representation among fauna would also be anticipated. Again, this represents a promising arena for new research, as we try to understand and predict how savanna structure and functioning are likely to change. We are starting to accumulate knowledge as to how small animals respond to the changes being brought to savannas by anthropogenic influences. We should be able to now string these together to erect some testable hypotheses as to how ecosystem structure and functioning is changing. This will allow formulation of management guidelines. Certainly, research to date suggests that management should try to mimic natural systems at the larger scale (i.e. with fire regimes, browsing, and grazing by larger mammals) as far as possible, in an attempt to ensure that the population dynamics of various small animals allow for optimum savanna functioning. References

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