**3. Terrestrial ecosystems**

of view, a growing body of evidence suggests that the evolutionary and ecological importance of herbivory occurs in an aquatic context as in terrestrial habitats [9, 11]. Interactions between herbivores and aquatic plants have been reported in a wide range of habitat types, including freshwater lakes, rivers, estuaries, wetlands, and shallow seas [26, 27]. Accordingly, interactions between herbivores and aquatic plants have global distribution, and herbivores are present wherever submerged, floating, or emergent plants are present [27]. It is a fact that aquatic herbivores have a strong impact on aquatic plant biomass, productivity, and species composition [22, 28]; thus, like in terrestrial angiosperms, selection may favor aquatic plants

Defense and resistance mechanisms against herbivores have been poorly understood in freshwater; even so we now know that freshwater plants are frequently chemically or structurally defended from consumers [29–31]. Structural defenses are more commonly found among upland plants than wetland plants [22]; in some cases, we can find thorns or tough leaves [32]. Chemical defenses are more widespread in macrophytes [23, 31] as well as in various algae,

Diverse groups of chemical compounds are known in aquatic plants, including alkaloids [33, 34], flavonoids, steroids, saponins, phenolics (including tannins), cyanogenic glycosides, glucosinolates [23, 29], quinines, and essential oils [32]. The different types of chemical defenses can vary between species, localities, time, and environmental conditions [31]. Many of them have not been identified; some studies have found multiple dissuasive components in the chemical extracts analyzed, but the low concentrations or their unstable state makes their identification difficult and therefore their correlation with the dynamics of the aquatic com-

In the aquatic environment, plant-herbivore interactions are different from terrestrial ecosystems because water provides different physicochemical conditions compared with air or soil, which should affect the herbivore access and the dispersal of released compounds [36].

The growth forms of macrophytes are the most significant adaptation to freshwater environments and have important consequences for aquatic plant-herbivore interactions. The structure of the macrophytes and the presence of leaves and flowers above or below the water level determine the access and type of herbivores [36], so structures above the water surface can be consumed by terrestrial herbivores while the submerged parts by aquatic herbivores. Therefore the growth forms may have different mechanisms to prevent herbivory. Compared with terrestrial vegetation, freshwater aquatic plants produce less phenolic compounds, and a different phenolic amount in the aquatic growth forms has been observed. Lodge [22] indicated that the rank of mean phenolic content in wetland plants is tree > floating leaves plants > emergent > submersed > algae. Submerged macrophytes have much lower content than emergent or floating leaved macrophytes [37]. These differences are because emergent plants need more structural tissue, thicker cell walls, and a more complex cuticle to limit evapotranspiration and provide stability; therefore they present structural defenses, while submerged

that have chemical and other types of antiherbivore defenses [9].

cyanobacteria [22].

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munity [35].

*2.2.1. Macrophyte growth adaptations*

The ancestors of terrestrial plants are closely related with charophytes. Plant terrestrialization was preceded by terrestrial algae after aquatic algae, with adaptive mechanisms to live in terrestrial environment such as drought, resistance to UV radiation. In addition, land plants need to increase its body size and cellular differentiation [41].

Another important topic is defensive mechanisms. Aquatic plants have only a few defensive compounds, and their structural defenses are limited because its biomass is constantly renewable. By contrast, terrestrial plants have a plethora of both chemical and structural defensive traits elaborate and accumulate by long-time periods [42]. Nevertheless, at different environment conditions, plants can accumulate diverse molecules or develop distinct structural mechanisms.

Abiotic factors, such as altitude, drought, and nutrient availability, can control defensive traits in plants. At altitudinal gradient, it has been hypothesized that the plant species growing at lower elevations need to invest more in defensive traits because they have greater herbivore pressure, whereas high-elevation plants need less defensive traits [43]. So, as expected at tropical forest, there are more defensive traits than at temperate forest.

Drought slows growth to decrease photosynthetic rate and, in moderate drought, an increase in secondary metabolites is possible, including defensive compounds and structures [44]. In tropical forest, the humidity remains relatively constant, then that factor is not significant.

Plant defense mechanisms are partially due to resources availability; at high resource availability, there are more photosynthesis and growth; but at low resource environments, plant increased defense allocation, because with herbivore attack, it is much more difficult to replace tissue [6, 45, 46].

#### **3.1. Temperate forest**

In temperate perennial forest, dominant plants are gymnosperms (see **Figure 1** for distribution). Conifers are dominant vegetation since 200 million years ago, and they appeared 300 million year ago, and during their evolution, they have had few changes. Currently, there are 630 species, which dominate many terrestrial ecosystems, principally in the Northern Hemisphere [47].

Gymnosperms are the major plant lineage with less leaf herbivory, only 0.9%. Low percentage can be explained to tough needle tissue and the presence of terpenoid resins [48]. Herbivory is low in temperate forest tree canopies, and the highest foliar damage occurs in high-quality leaves as youngest [49], it is more probably that the trunk is attacked by bark beetles [3].

At conifer communities, the primary compounds in defense are principally phenolics, terpenoids, and alkaloids, which lay up in the bark [50]. Another line of defense is resin ducts, which confer resistance to insect attack by resin production, flow, and chemical content (**Table 1**) [51].

There are two defense kinds: constitutive, which are expressed all time, even when they are not suffering from damage and induced defenses that enhanced after damage [50, 52]. Among constitutive defenses are resin canals, chemical compounds such as phenolics and therpenes, and the mechanical properties of the cortex that act as a barrier [50, 53]. Those constitutive compounds are nonselective against herbivores, but chemicals produced by induced defense

**Figure 1.** General distribution of different ecosystems in the world.


**Table 1.** Chemical compounds produced by principal plant types at different environments.

**3.1. Temperate forest**

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Hemisphere [47].

(**Table 1**) [51].

**Figure 1.** General distribution of different ecosystems in the world.

In temperate perennial forest, dominant plants are gymnosperms (see **Figure 1** for distribution). Conifers are dominant vegetation since 200 million years ago, and they appeared 300 million year ago, and during their evolution, they have had few changes. Currently, there are 630 species, which dominate many terrestrial ecosystems, principally in the Northern

Gymnosperms are the major plant lineage with less leaf herbivory, only 0.9%. Low percentage can be explained to tough needle tissue and the presence of terpenoid resins [48]. Herbivory is low in temperate forest tree canopies, and the highest foliar damage occurs in high-quality leaves as youngest [49], it is more probably that the trunk is attacked by bark beetles [3].

At conifer communities, the primary compounds in defense are principally phenolics, terpenoids, and alkaloids, which lay up in the bark [50]. Another line of defense is resin ducts, which confer resistance to insect attack by resin production, flow, and chemical content

There are two defense kinds: constitutive, which are expressed all time, even when they are not suffering from damage and induced defenses that enhanced after damage [50, 52]. Among constitutive defenses are resin canals, chemical compounds such as phenolics and therpenes, and the mechanical properties of the cortex that act as a barrier [50, 53]. Those constitutive compounds are nonselective against herbivores, but chemicals produced by induced defense

have a wide spectrum and form specific compounds, so they are very diverse and cover a great variety of herbivores [54, 55]. Among induced defenses include phenolic compounds, resin terpenoids, enzymes, PR proteins, and reactive oxygen species [50].

In conifers, resin terpenoids are produced during and after attack of insects, when constitutive duct is active and produces resin, which can flow at great quantity [54, 56].

The bark of conifers has abundant phenolic compounds [57–59]. When phenolics and tannins join to amino acids and proteins, both of them reduce the nutritional value and the ability of insects to digest plant tissues [60]. Constituent phenols can be converted in polyphenolic compounds after herbivore attack, and they are more toxic and specific against herbivores [61].

There are proteins than act as chemical defenses, such as enzymes that degrade components of herbivores such as glucanases and chitinases [62]. Generally, chemical defenses have multiple strategies overlapping that result in a chemical toxic cocktail that stops or destroys an aggressive or virulent attack.

At gymnosperms, multiple overlaying defense systems provide an efficient barrier against a wide range of possible insect attacks. However, conifers remain susceptible to certain organisms that have evolved strategies to overcome the defenses or avoid them. Nevertheless, the remarkable longevity of conifers is a proof to the success of their defense strategies (**Figure 2**) [53].

Another plant community at temperate environment is deciduous forest, particularly the oak forest (distribution in **Figure 1**). In *Quercus robur*, phenolic concentration in leaves increases toward higher elevations with a decrease in leaf damage in comparison with organism at same species that grow in lower altitude [43] that suggest that temperate oak forest is less susceptible to insect damage that tropical forest. In the same way, *Quercus variabilis* total phenolic and total condensed tannin concentration decreases to higher elevation and is more concentrated in juvenile individuals [63].





**Figure 2.** Characteristics related to defense mechanisms in plants of different environments.

In a temperate deciduous forest at Powdermill Nature Reserve, the leaf damage caused by herbivores and in majority of individual had a low rate than 2% that can be due to low herbivore densities and poor degrees of specialization thereof [64].

Also, in stressful environment like high-elevation alpine plant communities with low temperatures, plant species have asexual reproduction by rhizomes resulting in clones. Clonal species have developed a tolerance strategy against herbivores and reduced investment in chemical defense [65].
