Relationships (y = a + bx) of intake rates, leaf accessibility indices (LAIN), thorndensity and leaf size (y) of five woody species in a semi-arid southern African savanna and various browse intake rate parameters (x) achieved by goats when browsing on these plants (
Savannas cover more than ten percent of the world’s land surface and more than fifty percent of Africa, providing browse to millions of mammalian herbivores (Scogings & Mopipi, 2008). Although herbivory is a major driver of ecosystem functioning in semi-arid African savannas plant-herbivore interactions are poorly understood (Skarpe, 1992; Scholes, 1997; Scogings, 2003). African savannas and large herbivores coevolved, with woody plants developing defences against herbivory (Du Toit, 2003). The herbivores have in turn evolved counter measures against the plant defences. Large herbivores counteract the effects of plant defence by selective foraging, fragmentation of intact plant tissues, microbial fermentation and expanded guts for microbial breakdown, whereas plants protect themselves through morphological, structural and chemical adaptations (Borchard et al., 2011). African savanna ecosystems under heavy browsing have few hardy woody species that are resistant to or are defended against defoliation. Cornell and Hawkins (2003) suggested that plants acquire better defences with time which herbivores in turn learn to partly or fully overcome. Hartley & Jones (1997) found woody plants to be able to live in environments where herbivores were common because of their ability to resist or recover from intense herbivore pressure. The varying defences that plants exhibit is a reflection of the diversity of herbivores and abiotic conditions. Plant defences exert selective pressure on mammalian herbivores, with the result that many have developed mouthparts and digestive systems that facilitate the use of particular plant types. The chemical defences of terrestrial plants reflects in part the biochemical evolution of early land plants and the problems those plants encountered.
A number of plant defence theories have been advanced to explain why some plants are better defended than others. For example, the optimal defence hypothesis focuses on how defensive needs of plants leads to the evolution of chemical defences, with the cost of that defence maximizing fitness. This chapter will discuss the effects of herbivory on woody plants, show how the plants respond to herbivory and explore herbivore adaptations to plant defences. I will also discuss the woody plant-herbivore interactions in terms of browse instantaneous intake rates and explain how shoot morphology influences herbivory.
2. Effects of herbivory on woody plants
Herbivory can negatively through instantaneous death (Belsky, 1986) or positively through increased growth and competitive ability (McNaughton, 1979) influence plant fitness. The effect of herbivory on woody plants depend on the intensity and frequency of damage, plant phenological stage and resource relationships at the time of herbivory, plant tissues removed, competition with non-browsed species and the characteristics of the plant species (Maschinski & Whitham, 1989). Damage to individual woody plant branches negatively affects growth and reproduction of those branches but leads to compensatory growth in non damaged branches (Du Toit et al., 1990). Many woody species in the semi-arid savanna are able to resprout following herbivory. For example,
Under-compensation of lost biomass may prevent further browsing while full- or over-compensation may increase forage availability and quality and thus initiate further browsing (Bowyer & Bowyer, 1997). Dube et al. (2009) also reported
Herbivory during the early growth season coincides with nutrient flush enabling plants to benefit from energy mobilized from stored reserves. Scogings (2003) found defoliation during the early growth season to stimulate plant growth while growth of once-defoliated trees was not elevated above that of undefoliated trees when defoliation took place during the dormant season. Teague & Walker (1988) reported
Removal of the main shoots during browsing reduces apical dominance leading to the development of lateral shoots from activated dormant buds. Twig browsing in woody species can remove significant proportions of meristems resulting in fewer shoots in the following growth season (Bergstrom et al., 2000). The remaining shoots will experience less competition and thus grow larger and have higher nutrient concentrations than those on undamaged trees (Bergstrom et al., 2000; Rooke et al., 2004). Teague & Walker (1988) reported the increases in leaf and shoot of
Browsing reduces tree density, canopy cover and canopy diameter (Noumi et al., 2010) and affects tree regeneration (Mekuria et al., 1999). Fornara & du Toit (2008) reported
Shoot regrowths after defoliation have higher crude protein, phosphorus and biomass leading to repeated herbivory (Makhabu & Skarpe, 2006). Repeated browsing by megaherbivores such as the African elephant (
Herbivory may interfere with sexual reproduction in plants, either indirectly by changing physiology and allocation of resources, or directly by consumption of flower buds during the dormant season and flowers and fruits during the growth season (Skarpe & Hester, 2008; Fornara & du Toit, 2008). Herbivory results in plants allocating more resources to vegetative growth at the expense of sexual reproduction favouring species that reproduce vegetatively (Crawley, 1997). Goheen et al. (2007) reported herbivory as negatively affecting
3. Woody plant response to herbivory
Woody plants have evolved different strategies to reduce the negative effects of herbivory on their fitness (Rosenthal & Kotanen, 1994; Strauss & Agrawal, 1999). The strategies employed by plants to cope with herbivory can be classed into tolerance and avoidance mechanisms.
Tolerance strategies minimise the impacts of the damage (Hanley et al., 2007), with tolerant plants being generally palatable to the herbivores (Skarpe & Hester, 2008). Woody plants show tolerance to herbivory through morphological means such as quick replacement of lost leaves and shoots from protected meristems or through physiological processes such as compensatory photosynthesis and high and flexible rates of nutrient absorption (Hester et al., 2006). Re-sprouts have higher photosynthetic rates than older leaves. Teague (1989) reported
Plants avoid being consumed by employing structural deterrents such as spines and thorns, biochemical compounds such as proanthocyanidins (condensed tannins) and internal constitutive defences such as lignin and cellulose, which also act as structural support. Lignin influences the physical toughness and digestibility of plants reducing intake rates (Jung & Allen, 1995; Scogings et al., 2004; Shipley & Spalinger, 1992). The structural deterrents are defined as spines when they are made of leaves and thorns when they are made of branches (Raven et al., 1999). Spines and thorns are the first line of defence against herbivores foraging on most woody plants in semi-arid savanna. They provide mechanical protection through injuring herbivores’ mouths, digestive systems and other body parts. The presence of spines and thorns reduces the rate of herbivory by impeding stripping motions and forcing the herbivore to eat around the defence (Myers & Bazely, 1991; Wilson & Kerley, 2003a). Spinescent woody plants also have small leaves further reducing herbivore foraging efficiency since the reward received is seldom worth the time or energy needed to exploit it (Belovsky et al., 1991; Gowda, 1996). Plant spinescence increases with exposure to herbivory by large browsers as an induced defence (Milewski et al., 1991). Spines and thorns protect both leaves and axillary meristems (Gowda, 1996). Spine and thorn removal experiments have been carried out to demonstrate the protective value of these structures (Wilson & Kerley, 2003b; Hanley et al., 2007). Milewski et al. (1991) reported the removal of
Avoidance strategies also involve keeping most edible biomass beyond the reach of terrestrial herbivores. This means that the plant will have to survive herbivory before growing beyond the reach of the browsers. Woody plants growing in nutrient–rich environments are likely to grow above browsing height for most herbivores faster than trees in nutrient-poor environments, which will suffer browsing for a longer period (Danell et al., 1997). Woody plants growing in nutrient-poor environments have slow growth rates that limit their capacity to grow rapidly beyond the reach of most browsing mammals. They have developed strong defences for protection against herbivory (Coley et al., 1985; Teague, 1989; Borchard et al., 2011). Woody plants that grow in resource-rich environments often do not avoid herbivory, but develop tolerance traits to minimize the harmful effects of herbivory (Skarpe & Hester, 2008).
Storage of carbohydrates reserves in woody stems or underground is also a kind of escape strategy. Plants may also escape herbivory by association with either less palatable or more palatable species, depending on the foraging pattern of the herbivore (Hjalten et al., 1993; Hester et al., 2006). When palatable plants gain protection from their unpalatable neighbours the phenomenon is referred to as associational defence (McNaughton, 1978; Hjalten et al., 1993). However, palatable plants are usually susceptible to attack when they occur in a patch with unpalatable neighbours, a situation referred to as neighbour contrast susceptibility (Bergvall et al., 2006).
Plants do not respond passively to damage by herbivory. The optimal defence hypothesis predicts increases in defences in direct response to herbivory (Rhoades, 1979). Herbivore attack leads to decreased acceptability and plant nutritional quality (Malecheck & Provenza, 1983; Rhoades, 1985; Lundberg & Astrom, 1990). Plant defences will either reduce consumption rates or reduce the ability of herbivores to digest material once consumed (Belovsky et al., 1991; Robbins, 1993). Plants damaged by herbivores prevent further damage through an increase in digestion inhibiting compounds such condensed tannins (Cooper & Owen-Smith, 1985) and an increase in structural deterrents such as spines and thorns (Milewski et al., 1991). Some African woody species such as
Both avoidance and tolerance involves costs for the plant such as in the building and maintenance of stores of energy and nutrients as well as of dormant buds that can be activated following herbivory (Bilbrough & Richards, 1993). Plant defences compete with growth and reproductive requirements for nitrogen and carbohydrate resources (Hanley et al., 2007). Owen-Smith & Cooper (1987) reported fewer plants as investing in both chemical and structural anti-herbivore defences to reduce costs to growth and reproduction.
4. Herbivore adaptations to plant defences
Herbivores need to develop ways of counteracting plant defences in order to utilise woody plants as browse (Hanley et al., 2007). Herbivores that forage on spinescent plants have smaller mouthparts to deal with the intricate task of removing small leaves from between dense assemblages of spines and thorns (Belovsky et al., 1991). Most browsing animals have agile lips and tongues that allow them to select leaves and avoid thorns (Gordon and Illius, 1988). For example goats with their mobile and narrow muzzle, can manoeuvre their mouths more easily among thorns to pluck small leaves, making thorns less effective in reducing cropping rates (Shipley et al., 1999; Cooper & Owen-Smith, 1986). Giraffe (
The evolution of a ruminant stomach can also be considered as an adaptation to plant defences since this allows the ungulates to digest fibrous plant material (Perez-Barberia et al., 2004). The ungulate stomach has symbiotic microorganisms and also releases cellulase enzymes which break down cellulose-rich cell wall fractions of plant material releasing volatile fatty acids that are immediately absorbed by the stomach (Hanley et al., 2007).
Some herbivores are able to develop behavioural and physiological counter adaptations against chemical plant defences (Iason & Villalba, 2006). For example, browsers such as goats secrete tannin-binding salivary proteins which counter the digestibility-reducing effect of ingested condensed tannins (Robbins et al., 1987). Tannin-binding salivary proteins contain a high proportion of proline, and proline-rich salivary proteins have a greater binding affinity for tannins than other proteins, and thus act to prevent tannins from interacting with other proteins in mammalian digestive systems (Shimada, 2006). The production of proline-rich proteins enhances cell wall (fiber) digestion of high-tannin forages by ungulates (Robbins et al., 1987).
5. Browse instantaneous intake rates
The foraging efficiency of browsers on different woody species can be defined in terms of the instantaneous intake rate (Wilson & Kerley, 2003b). Browse instantaneous intake rate is a product of bite size and bite rate and is influenced by plant characteristics. Different browse species will allow browsers to crop varying number and size of bites leading to highly variable instantaneous intake rates. Illius & Gordon (1990) estimated that browsers crop between 10 000 and 40 000 bites per day from different individual plants. Decisions made by the browser when selecting a bite have important consequences for its nutritional intake and hence fitness (Shipley et al., 1999). Most woody plants with nutritious forage have thorns or spines (Wilson & Kerley, 2003b). In semi-arid and arid African savannas thorny plants occur in areas with many large browsers (Grubb, 1992). Plant characteristics such as leaf size, thorn density and inter-thorn spacing (leaf accessibility) affect instantaneous intake rates through their effects on bite size and bite rate (See Table 1).
|a) Intake rate vs|
b) LAIN vs
c) Thorn density vs
d) Leaf size vs
y = 20.87 + 3.02x
y = 36.09 + 7.35x
y = 0.14 + 0.03x
y = 4.97 + 1.63x
y = 0.12 – 0.03x
y = 31.79 – 6.42x
y = 3.86 – 1.70x
y = 0.87 + 0.20x
y = 0.05 + 0.05x
y = 22.2 + 7.13x
To achieve higher instantaneous intake rates browsers have to select browse species that allow large bite sizes and higher bite rates. Thus factors that constrain both bite size and bite rate will reduce instantaneous intake rates. Leaf accessibility and leaf size positively influenced bite size while thorn density had a negative effect (Table 1). Species with higher leaf accessibility allowed higher bite rates as the goats could easily maneuver their mouths between thorns when plucking the leaves. Thorns restricted goat muzzle movement slowing down the rate of browse harvesting (Belovsky et al., 1991). Thorns also force browsers to change foraging strategy from twig biting and leaf stripping to the less detrimental picking of leaves from between the thorns (Cooper & Owen-Smith, 1986; Gowda, 1996), reducing the loss of foliage to mammalian browsers. Browsers will achieve higher instantaneous intake rates through selecting species with higher leaf accessibility and larger leaves. However, handling time increases with increasing leaf size, suggesting that there is an optimum leaf size (Wilson & Kerley, 2003a).
6. Relationship between shoot morphology and herbivory
Shoot morphology has an influence on how plants protect themselves against loss of valuable nutrients and photosynthetic tissue to herbivores (Sebata & Ndlovu, 2012). Scogings et al. (2004) reported defences as being distributed among woody plants in semi-arid savannas according to shoot morphology because it affects the vulnerability of plant parts to browsers. Woody plants can be divided into two groups
The shoot-limited species are poorly defended chemically and depend on structural defences (thorns) which the goats are able to avoid using their mobile upper lips. Shoot-limited species have lower contents of plant secondary compounds (condensed tannins and fibre) and higher digestibility and rumen fermentation than shoot-limited species (Sebata & Ndlovu, 2012). Fibre enhances leaf toughness and reduces browsing (Jung & Allen, 1995; Shipley & Spalinger, 1992). Shoot-limited species also rapidly replace lost tissues through regrowth (Scogings et al., 2004). Shoot-limited and shoot-dominated species are able to adapt different anti-herbivory defences.
Woody plants, at light stocking rates, are able to compensate biomass lost to herbivory. However, at high animal densities they may not be able to replace lost foliage, which could eventually lead to their mortality. Thus to maintain a positive herbivore-plant relationship ungulate populations in savanna ecosystems need to be regulated. Although herbivory stimulates woody plant resprouting, there is still need for defences against excessive defoliation. However, plant defences compete with growth needs requiring a balance in resource allocation. The allocation of nutrients and water resources to defence and growth is poorly understood necessitating further studies. The most effective herbivore adaptation to plant defences is selection of browse with low physical and chemical defences e.g. selecting shoot-limited over shoot-dominated woody species. The extent to which herbivore adaptations to plant defences allow ungulates to exploit the diverse woody plant resources needs to be studied. Woody plants in semi-arid savanna ecosystems are able to persist under intense herbivory due to key adaptations that include structural defences, chemical defences and compensatory growth abilities of the plants. The relationship between plant defences and high compensatory growth abilities of the plants are poorly understood. Structural defences are effective in limiting foliage loss to browsers and represent a cheap form of defence in semi-arid savannas.