**3. Botanical classification of resistance**

The botanical classification of life forms is very often, if not always, a challenge for agronomists. In order to understand how nature is reacting to the heavy load of herbicides continuously thrown into the environment, first there is a need to briefly understand the botanical classification and how plants are grouped.

The Biological Classification—or Taxonomic Rank—describes the level of a group of organisms into the taxonomic hierarchy [13]. The main taxonomic ranks are domain, kingdom, division, class, order, family, genus, and species, all of them with an internal classification prefixed by "sub" (subclass, subfamily, etc.) [14]. Other classification levels into each section may exist, but this is beyond an agronomist's point of view and will not be discussed in the present study.

#### **3.1. Botanical order**

In botany, "order" is a taxonomic rank located between "class" and "family," grouping plants with similar traits at a certain degree [14]. Even though several botanical orders exist, most weed species should be classified into approximately 20 orders. **Figure 3** depicts weed species distribution into orders, from combined data of the five studied countries (Australia, Brazil, Canada, France, and the United States).

**Figure 3.** Percentage of resistant weed species by botanical order, with pooled data from the five studied countries. Source: adapted from Heap [8].

The great majority of weed species resistant to herbicides are included into the orders Poales, Caryophyllales, Asterales, and Brassicales (**Figure 3**). For the four reference countries (**Figure 4**), the order Poales was the predominant one, as also seen for the overall order data (**Figure 3**). In Canada, the importance of this order was shared with Caryophyllales, which was the second most important resistant weed group in France. Asterales was of importance also in Australia and the United States while it was of secondary importance in Canada and France (**Figure 4**). Overall, 10, 8, 6, and 12 orders including resistant weed species were identified in Australia, Canada, France, and the United States, respectively.

pulp are also cultivated. Moreover, the paper industry is also important in the country [11]. As the world's sixth largest economy, Brazil ranks third among the world's major agricultural exporters and fourth for food products, being the world's largest producer and exporter of products such as

Thus, there is a great difference between the major crops grown in France and Brazil, which is probably the cause for a distinct herbicide demand and, as consequence, the difference in

The botanical classification of life forms is very often, if not always, a challenge for agronomists. In order to understand how nature is reacting to the heavy load of herbicides continuously thrown into the environment, first there is a need to briefly understand the botanical

The Biological Classification—or Taxonomic Rank—describes the level of a group of organisms into the taxonomic hierarchy [13]. The main taxonomic ranks are domain, kingdom, division, class, order, family, genus, and species, all of them with an internal classification prefixed by "sub" (subclass, subfamily, etc.) [14]. Other classification levels into each section may exist, but this is beyond an agronomist's point of view and will not be discussed in the present study.

In botany, "order" is a taxonomic rank located between "class" and "family," grouping plants with similar traits at a certain degree [14]. Even though several botanical orders exist, most weed species should be classified into approximately 20 orders. **Figure 3** depicts weed species distribution into orders, from combined data of the five studied countries (Australia, Brazil,

**Figure 3.** Percentage of resistant weed species by botanical order, with pooled data from the five studied countries.

soybean, coffee, sugarcane, orange juice, meat, and tobacco [12].

nature of resistance cases between these two countries.

**3. Botanical classification of resistance**

138 Herbicide Resistance in Weeds and Crops

classification and how plants are grouped.

Canada, France, and the United States).

**3.1. Botanical order**

Source: adapted from Heap [8].

In Brazil, the most important weed species are included into the botanical orders Poales, Asterales, and Caryophyllales (**Figure 5**). In general, these findings are according to the data observed for the four reference countries (**Figure 4**), where these three botanical orders also tended to predominate.

There are five, four, three, and six botanical orders, respectively, in Australia, Canada, France, and the United States, with resistant biotypes (**Figure 4**), which are still absent in Brazil (**Figure 5**). Among the plant orders with resistant biotypes, Solanales is present in the four reference countries, whereas Lamiales and Gentianales are present in Australia and Canada (**Figure 4**). The order Solanales includes botanical families with important weed species in Brazil like Solanaceae and Convolvulaceae; Lamiales includes the families Plantaginaceae and Lamiaceae, while Gentianales includes the family Rubiaceae [14].

**Figure 4.** Wordcloud for the occurrence of weed resistance as a function of botanical order in the reference countries. The scale of the font represents the importance of the order compared to the others in the same figure. Source: adapted from Heap [8].

**Figure 5.** Wordcloud for the occurrence of weed resistance as a function of botanical order in Brazil. The scale of the font represents the importance of the order compared to the others in the same figure. Source: adapted from Heap [8].

It should be emphasized that in the present study, the classification of weeds in botanical orders is restricted to those species considered as "weed" in the agricultural context; this does not mean at all major number of plant species included in that order are most prone to become a weed. This relationship is yet to be established, supposing it exists.

#### **3.2. Botanical family**

Resistant weeds grouped by botanical family (**Figure 6** and **Figure 7**) showed Poaceae as the major family with resistant species for all studied countries, including Brazil. In Australia, Brassicaceae and Asteraceae families were in the second and third places, respectively; in Canada, Amaranthaceae was the family with the most number of plant species with resistant biotypes to herbicides followed by Brassicaceae, Asteraceae, and Chenopodiaceae (**Figure 6**). In France, Asteraceae, Amaranthaceae, and Polygonaceae were also important botanical families in number of weeds with resistant biotypes, and in the United States, Amaranthaceae and Asteraceae were highlighted after Poaceae (**Figure 6**).

In Brazil, Asteraceae and Amaranthaceae were the predominant families of plants with resistant weed biotypes after Poaceae (**Figure 7**).

Compared to the reference countries, from one point of view, there is danger in Brazil under the current panorama of herbicides use and weed management—for an increase in the

**Figure 6.** Wordcloud for the occurrence of weed resistance as a function of botanical family in the reference countries. The scale of the font represents the importance of the family compared to the others in the same figure. Source: adapted from Heap [8].

It should be emphasized that in the present study, the classification of weeds in botanical orders is restricted to those species considered as "weed" in the agricultural context; this does not mean at all major number of plant species included in that order are most prone to become

**Figure 5.** Wordcloud for the occurrence of weed resistance as a function of botanical order in Brazil. The scale of the font represents the importance of the order compared to the others in the same figure. Source: adapted from Heap [8].

Resistant weeds grouped by botanical family (**Figure 6** and **Figure 7**) showed Poaceae as the major family with resistant species for all studied countries, including Brazil. In Australia, Brassicaceae and Asteraceae families were in the second and third places, respectively; in Canada, Amaranthaceae was the family with the most number of plant species with resistant biotypes to herbicides followed by Brassicaceae, Asteraceae, and Chenopodiaceae (**Figure 6**). In France, Asteraceae, Amaranthaceae, and Polygonaceae were also important botanical families in number of weeds with resistant biotypes, and in the United States, Amaranthaceae and

In Brazil, Asteraceae and Amaranthaceae were the predominant families of plants with resis-

Compared to the reference countries, from one point of view, there is danger in Brazil under the current panorama of herbicides use and weed management—for an increase in the

a weed. This relationship is yet to be established, supposing it exists.

Asteraceae were highlighted after Poaceae (**Figure 6**).

tant weed biotypes after Poaceae (**Figure 7**).

**3.2. Botanical family**

140 Herbicide Resistance in Weeds and Crops

number of resistant plant biotypes mainly from the families Asteraceae, Amaranthaceae, and Brassicaceae, which are significant in the reference countries and, at the same time resistant, biotypes were already reported in Brazil.

Second, there is also a great chance for the appearance of resistant weed biotypes from families which are absent in the current Brazilian scenario, but which have great importance in all four reference countries, like Polygonaceae and Solanaceae, or in three out of the four reference countries like Chenopodiaceae and Caryophyllaceae (**Figure 6**).

A third scenario leads to the increasing number of multiple resistance or the appearance of resistance to a second herbicidal mechanism of action in weed species which are already resistant to a given mechanism of action [6]. This is concerning due to the nature of the new technologies of crop tolerance to herbicides, the so-called "all-in-one" tolerance; crops will have tolerance to more than one herbicide mechanism of action [15]. Thus, weeds will have to "tolerate" or "resist" to most of the herbicides associated to each technology, in order to prevail in arable fields.

One should note that there was an initial attempt to predict future cases of weed resistance in Brazil [16], by analyzing the herbicidal mechanism of action to which some plant

**Figure 7.** Wordcloud for the occurrence of weed resistance as a function of botanical family in Brazil. The scale of the font represents the importance of the family compared to the others in the same figure. Source: adapted from Heap [8].

species evolved resistance in some parts of the world, and relating the risk for new cases to the adoption of such herbicides in Brazilian agriculture. This analysis [16] was, however, excluded in the updated version of the same book [15] but may be considered as complementary to the present study, even being outdated by some degree.

When the evolution of appearance of families with resistant biotypes was analyzed by countries (**Figure 8**), it was observed that the most important botanical family in number of resistance cases is Poaceae (**Figure 6** and **Figure 7**), which was the first to appear in Australia, in 1982; the second in France and the United States in 1978 and 1970, respectively; and the sixth botanical family to have resistant biotypes in Canada (**Figure 8**).

The other botanical families with resistant biotypes with great importance that were reported in the reference countries (**Figure 6**) are listed in the inset table in **Figure 8**. It is important to note that the most important botanical families were also, in general terms, between the first ones to appear in the respective countries. This leads to the hypothesis that these families are of relatively recent evolutionary origin [5]. There is evidence that the preponderance of weeds from relatively recent evolutionary origin indicates the trend to an increasing of troublesome, highly adaptable weeds in agriculture [5, 7]. An example is the botanical family Asteraceae [7], which already has resistant biotypes in the five countries studied here (**Figure 5** and **Figure 7**). Thereby, in the years to come, Brazil may experience an increase in the occurrence of weed species from families with recent evolutionary origin.

**Figure 8.** Evolution of resistant botanical families by year and country, with an inset table showing the number of families in each reference country with resistant biotypes, and the number of these families that are present in Brazil, with or without resistant biotypes. Source: adapted from Heap [8].

**Figure 9** illustrates the geographic distance between Brazil and the reference countries used in this study. In general terms, half or less than half of the families present in the reference countries are also present in Brazil with resistant biotypes. This may lead to the assumption that there is still plenty of species to evolve resistance in Brazil, supposing that farmers and technicians will keep relying heavily on the chemical weed control, in absence of alternative weed management techniques.

species evolved resistance in some parts of the world, and relating the risk for new cases to the adoption of such herbicides in Brazilian agriculture. This analysis [16] was, however, excluded in the updated version of the same book [15] but may be considered as complemen-

**Figure 7.** Wordcloud for the occurrence of weed resistance as a function of botanical family in Brazil. The scale of the font represents the importance of the family compared to the others in the same figure. Source: adapted from Heap [8].

When the evolution of appearance of families with resistant biotypes was analyzed by countries (**Figure 8**), it was observed that the most important botanical family in number of resistance cases is Poaceae (**Figure 6** and **Figure 7**), which was the first to appear in Australia, in 1982; the second in France and the United States in 1978 and 1970, respectively; and the sixth

The other botanical families with resistant biotypes with great importance that were reported in the reference countries (**Figure 6**) are listed in the inset table in **Figure 8**. It is important to note that the most important botanical families were also, in general terms, between the first ones to appear in the respective countries. This leads to the hypothesis that these families are of relatively recent evolutionary origin [5]. There is evidence that the preponderance of weeds from relatively recent evolutionary origin indicates the trend to an increasing of troublesome, highly adaptable weeds in agriculture [5, 7]. An example is the botanical family Asteraceae [7], which already has resistant biotypes in the five countries studied here (**Figure 5** and **Figure 7**). Thereby, in the years to come, Brazil may experience an increase in the occurrence of weed species from families with recent evolutionary origin.

tary to the present study, even being outdated by some degree.

142 Herbicide Resistance in Weeds and Crops

botanical family to have resistant biotypes in Canada (**Figure 8**).

**Figure 9.** Correlation in the occurrence of botanical families of weeds between Brazil and the reference countries, and its proportion of families which already present resistant biotypes in Brazil. Source: adapted from Heap [8].

#### **3.3. Botanical genera**

The botanical genera with resistant species in the reference countries are shown in **Figure 10**. In Australia, *Lolium* was the predominant genus in number of resistant weed species; in Canada and the United States, *Amaranthus* is the most important one; in France, there is no predominant genus with the most cases of resistant weed biotypes being *Avena, Amaranthus, Lolium, Setaria*, and *Echinochloa* similar in importance (**Figure 10**). In Australia, *Raphanus, Bromus, Hordeum, Avena*, and *Sisymbrium* are the second most important group of genera with resistant weed biotypes; in Canada, *Setaria* and *Avena* are also in the second group. In the United States, a great number of botanical genera with resistant weed biotypes occur, but *Echinochloa, Conyza, Poa, Setaria, Kochia, Ambrosia*, and *Lolium* may be highlighted in a second group of importance, following *Amaranthus*.

In Brazil, 19 genera with resistant biotypes are reported (**Figure 11**), where *Amaranthus, Conyza*, and *Bidens* are the most important ones, followed by *Digitaria, Lolium*, and *Echinochloa* in the second group. A third group includes *Sagittaria, Euphorbia, Eleusine, Cyperus*, and *Raphanus*.

**Figure 10.** Wordcloud for the occurrence of weed resistance as a function of botanical genus in the reference countries. The scale of the font represents the importance of the genus compared to the others in the same figure. Source: adapted from Heap [8].

**Figure 11.** Wordcloud for the occurrence of weed resistance as a function of botanical family in Brazil. The scale of the font represents the importance of the genus compared to the others in the same figure. Source: adapted from Heap [8].
