*of its turret, the nymph therefore has a register of behaviours specific to the function performed*.

The most common method of opening before moulting (named program A) is worth explaining here. It takes place in two phases: a draft of the opening (**Figure 15a–c**), then an equalisation until the opening is remarkably circular (**Figure 15d**).

Continuous monitoring makes it possible to describe in detail the behaviour of the nymph which creates the roughing by enlarging (**Figure 16a–c**) the initial perforation (**Figure 15a**) by a scraping carried out with the chitins' end of its forelegs, up to obtain an elongated opening with irregular edges (**Figure 16c**). Working from the inside, the nymph is almost invisible. When the roughing is complete, the nymph appears (**Figure 16c**) and undertakes the work of equalisation, which is accomplished by scraping the edge with the chitins' end of its forelegs

**101**

*The Nymph Architect of the Cicada* Guyalna chlorogena*: Behaviours and Ecosystem*

(fl) also (**Figure 16d**), at the same time as it performs rotations. During this phase, the nymph's head is clearly visible, and one can easily recognise its *antennae* (ant), *front legs* (fl) and *clypeus* (cly). Once the equalisation is complete (**Figure 16e**), the nymph disappears until its exit (**Figure 16f**) which takes place with a remarkable precision between 6 p.m. and 6:10 p.m. (local time). The 6 pictures in **Figure 17** illustrate the rotations that the nymph performs at the same time as it levels the edge

The monitoring of two individuals, from the exit of the nymph from its turret, until the flight of the imago, made possible to establish a detailed time schedule

Each time an edifice of *G. chlorogena* was discovered on the site we studied, an arborescent *Fabaceae* of the genus *Tachigali* has been identified in the vicinity (Béguin, Gama and Ribamar Mesquita Ferreira, to be published). The building of the nymph is usually the much farther from the tree the larger this one is. This fact is not surprising when one takes into account: 1°) that a cicada nymph can plant its tiny rostrum [4] to suck up the elaborate sap on which it feeds, only in radicular extremities of comparable size, close to the meristems; 2°) that the root ends of trees, in the Amazon rainforest where the layer of fertile soil is very small (of the order of 1 meter), instead of plunging in depth, spread out [5], forming a "root

During the 2 years 2018 and 2019, we identified 132 buildings of *G. chlorogena* distributed among 14 trees of the genus *Tachigali*; 11 from the species *chrysophyllum* and 3 from the species *venusta*. We therefore measured, for each building, the dis-

The results were reported on two graphs relating the diameter of a tree with: a) the distances to all the buildings associated with it (**Figure 18a**); b) the average distance to them (**Figure 18b**). The trend lines calculated with *Excel* by the smallest squares indicate clearly, on each of the graphs, a proportionality between the diameter of the trunk of the tree and its distance to a building of *G. chlorogena*, thereby providing a logical-mathematical support to the associa-

apparently being the main, if not the only, beneficiary of this relationship, we

The graph with plotting of all distances (**Figure 18a**) shows that part of the buildings are located near the trunk. We will be re-examining our statistics to determine if the location of the buildings is related to the *Tachigali* species (*chrysophyllum* or *venusta*). One thing is obvious; nymph buildings (i.e. nymphs feeding) close to the trunk involve root ramifications down to the level of the meristems from the proximal roots, particularly the buttresses. We recently discovered, at another place in the *Adolfo Ducke reserve*, a *Tachigali* station of a species (yet to be identified) which is neither *chrysophyllum* nor *venusta*, with nymph buildings (the species to which their hosts belong has not yet been confirmed as *G. chlorogena*) close to the trunk. In Santarém (*Pará*, Brazil), edifices of *Fidicina chlorogena*, a taxon since identified with *G. chlorogena* [1] have been described [7] near the base of the trunk; the

<sup>4</sup> It is due to this situation to meet, at the Botanical Garden of Manaus for example, buildings in a built

, as well as the diameter of the trunk of this latter3

.

. *G. chlorogena*

disc" whose radius is all the greater as the size of the tree is large.

tion between the nymphs of *G. chlorogena* and these *Fabaceae*<sup>4</sup>

admit that this is a case of *commensalism* [6].

<sup>2</sup> More precisely of the estimated center of its implantation surface.

area near the forest. This is the case with the one shown in **Figure 11**.

<sup>3</sup> If the trunk is connected to a buttress by its base, its diameter is measured above.

*DOI: http://dx.doi.org/10.5772/intechopen.94106*

of the opening with its forelegs.

tance separating it from the tree2

(**Table 1**).

**8. Ecosystem**

*The Nymph Architect of the Cicada* Guyalna chlorogena*: Behaviours and Ecosystem DOI: http://dx.doi.org/10.5772/intechopen.94106*

(fl) also (**Figure 16d**), at the same time as it performs rotations. During this phase, the nymph's head is clearly visible, and one can easily recognise its *antennae* (ant), *front legs* (fl) and *clypeus* (cly). Once the equalisation is complete (**Figure 16e**), the nymph disappears until its exit (**Figure 16f**) which takes place with a remarkable precision between 6 p.m. and 6:10 p.m. (local time). The 6 pictures in **Figure 17** illustrate the rotations that the nymph performs at the same time as it levels the edge of the opening with its forelegs.

The monitoring of two individuals, from the exit of the nymph from its turret, until the flight of the imago, made possible to establish a detailed time schedule (**Table 1**).

#### **8. Ecosystem**

*Ecosystem and Biodiversity of Amazonia*

First perforation for the opening of the top of the

Exit of the nymph through the opening at the top

*Work schedule of the nymph during its moult to imago.*

End of opening (before equalising the edge) -

**100**

*performed*.

**Table 1.**

**Figure 17.**

turret

program *A*

of its turret

(**Figure 15d**).

*of its turret, the nymph therefore has a register of behaviours specific to the function* 

*Six snapshots illustrating the nymph's rotations when equalising the edge of the opening with its forelegs. (a) 9:15 a.m. (b) 9:35 a.m. (c) 9:37 a.m. (d) 9:38 a.m. (e) 9:41 a.m. (f) 9:45 a.m.. Arrows represent the rotations from the previous snapshot;* ant*: Antenna,* fl*: Foreleg,* cly*: Clypeus. Observation on 01.09.2019.*

Equalisation of the edge completed - program *A* Between 10:00 and 12:00 a.m.

Immobilisation before moulting Between 6:45 and 7:00 p.m.

Downtime to moult About 2 hours Downtime after moulting (drying the wings) About 5 hours Taking flight After 2 a.m.

**Moulting period Late July - early September (maximum frequency** 

**during the first week of August)**

Between 8:30 and 11:00 a.m.

Between 6:00 and 6:10 p.m.

Before 7:00 a.m.

is worth explaining here. It takes place in two phases: a draft of the opening (**Figure 15a–c**), then an equalisation until the opening is remarkably circular

The most common method of opening before moulting (named program A)

Continuous monitoring makes it possible to describe in detail the behaviour of the nymph which creates the roughing by enlarging (**Figure 16a–c**) the initial perforation (**Figure 15a**) by a scraping carried out with the chitins' end of its forelegs, up to obtain an elongated opening with irregular edges (**Figure 16c**). Working from the inside, the nymph is almost invisible. When the roughing is complete, the nymph appears (**Figure 16c**) and undertakes the work of equalisation, which is accomplished by scraping the edge with the chitins' end of its forelegs

Each time an edifice of *G. chlorogena* was discovered on the site we studied, an arborescent *Fabaceae* of the genus *Tachigali* has been identified in the vicinity (Béguin, Gama and Ribamar Mesquita Ferreira, to be published). The building of the nymph is usually the much farther from the tree the larger this one is. This fact is not surprising when one takes into account: 1°) that a cicada nymph can plant its tiny rostrum [4] to suck up the elaborate sap on which it feeds, only in radicular extremities of comparable size, close to the meristems; 2°) that the root ends of trees, in the Amazon rainforest where the layer of fertile soil is very small (of the order of 1 meter), instead of plunging in depth, spread out [5], forming a "root disc" whose radius is all the greater as the size of the tree is large.

During the 2 years 2018 and 2019, we identified 132 buildings of *G. chlorogena* distributed among 14 trees of the genus *Tachigali*; 11 from the species *chrysophyllum* and 3 from the species *venusta*. We therefore measured, for each building, the distance separating it from the tree2 , as well as the diameter of the trunk of this latter3 .

The results were reported on two graphs relating the diameter of a tree with: a) the distances to all the buildings associated with it (**Figure 18a**); b) the average distance to them (**Figure 18b**). The trend lines calculated with *Excel* by the smallest squares indicate clearly, on each of the graphs, a proportionality between the diameter of the trunk of the tree and its distance to a building of *G. chlorogena*, thereby providing a logical-mathematical support to the association between the nymphs of *G. chlorogena* and these *Fabaceae*<sup>4</sup> . *G. chlorogena* apparently being the main, if not the only, beneficiary of this relationship, we admit that this is a case of *commensalism* [6].

The graph with plotting of all distances (**Figure 18a**) shows that part of the buildings are located near the trunk. We will be re-examining our statistics to determine if the location of the buildings is related to the *Tachigali* species (*chrysophyllum* or *venusta*). One thing is obvious; nymph buildings (i.e. nymphs feeding) close to the trunk involve root ramifications down to the level of the meristems from the proximal roots, particularly the buttresses. We recently discovered, at another place in the *Adolfo Ducke reserve*, a *Tachigali* station of a species (yet to be identified) which is neither *chrysophyllum* nor *venusta*, with nymph buildings (the species to which their hosts belong has not yet been confirmed as *G. chlorogena*) close to the trunk. In Santarém (*Pará*, Brazil), edifices of *Fidicina chlorogena*, a taxon since identified with *G. chlorogena* [1] have been described [7] near the base of the trunk; the

<sup>2</sup> More precisely of the estimated center of its implantation surface.

<sup>3</sup> If the trunk is connected to a buttress by its base, its diameter is measured above.

<sup>4</sup> It is due to this situation to meet, at the Botanical Garden of Manaus for example, buildings in a built area near the forest. This is the case with the one shown in **Figure 11**.

#### **Figure 18.**

*Relationship between Tachigali's trunk diameters and distances to G. chlorogena's edifices. (a) Plotting distances to all the buildings associated with a given tree. (b) Plotting the average distance to the buildings associated with a given tree.*

species name of the tree was not reported. The same disposition was observed [8] for *Orialella aerizulae* (Boulard), which could also feed on *Tachigali* sp. as well as possibly on *Tabebuia* sp. This aspect of the dependency relationship between cicadas and their foster trees has to be explored in more detail.

### **9. Reproductive cycle**

The nymphs spend several years underground, moving to reach the fine roots (less than 2 mm) from which they suck, with their rostrum, the elaborate sap on which they feed (see above). They move forward by digging galleries with their forelegs, throwing the excavated material behind them.

On can consider [9] the beginning of the reproductive cycle at the time of mating (**Figure 19a**), after the nymph has emerged from its burrow and moulted into an imago (**Figure 19h, i**). The winged adults, stimulated by singing males, mate in trees. Then the females search for a stem in which they will plant their ovipositor several times [10] to deposit their eggs under the bark (**Figure 19b**). The larvae hatch on the twigs and then fall to the ground (**Figure 19c**) where they sink (**Figure 19d**). No one has yet observed their behaviour during this first phase of underground life. No one either knows the duration of the underground life until the exit to moult into a winged imago; it is estimated at several years.

From excavations undertaken after moulding with cement (see above), which revealed an inclination of the deepest zone of the well, as well as in its vicinity traces of oblique galleries of intermediate inclinations (**Figure 5b**), one can envisage the upwards digging of a vertical well from a deep horizontal gallery (**Figure 19e**) by digging successive oblique galleries more and more inclined (**Figure 19f**).

The digging of deep horizontal galleries giving access to fine roots that the nymphs can use to feed themselves (see above), is consistent with the presence of a

**103**

nymph is placed in a glass tube.

*nymph comes out of the turret to turn into an imago.*

**10. Role of urine**

**Figure 19.**

after drying [13].

*The Nymph Architect of the Cicada* Guyalna chlorogena*: Behaviours and Ecosystem*

significant biomass of fine roots in the deep soil layer of the Amazon rainforest, as recent research has shown [11]. The digging of successive oblique galleries more and more inclined implies a capacity of the nymph to back up into an already dug burrow. Such a capacity is observed when one surprises, by the withdrawal of its turret, a nymph near the exit of its well. It can also be observed in experiments where the

*Life cycle of G. chlorogena. (a) Mating. (b) Lay eggs. (c) After hatching, the tiny larvae (~ 2 mm) fall to the ground. (d) They bury themselves in the ground. (e) The nymph digs its gallery at the same time as it feeds on the sap of the roots. (f) As it moves forward and back, the nymph changes direction until it is vertically oriented. (g) The nymph digs the well which is a vertical gallery. (h) the turret is built from the well. (i) The* 

The key role mentioned above of urine in *G. chlorogena*, has been underlined in connection with the construction of the turret and the various maintenance activities described; in experiments where the turret was replaced by a glass tube [2], the observation was made of the rise of the urine soaked mass of clay that the nymph loads on its head. The role of urine, in European species of cicadas, was demonstrated [12] for digging underground burrows; abdominal gutters redirect urine to the anterior part of the body and allow the nymph to use it to soften the soil with its forelegs. In the case of *G. chlorogena*, urine is used to soften the clay [2]. Urine from cicadas also contains *mucin*, a *glycoprotein*, which strengthens the walls of burrows

*DOI: http://dx.doi.org/10.5772/intechopen.94106*

*The Nymph Architect of the Cicada* Guyalna chlorogena*: Behaviours and Ecosystem DOI: http://dx.doi.org/10.5772/intechopen.94106*

#### **Figure 19.**

*Ecosystem and Biodiversity of Amazonia*

species name of the tree was not reported. The same disposition was observed [8] for *Orialella aerizulae* (Boulard), which could also feed on *Tachigali* sp. as well as possibly on *Tabebuia* sp. This aspect of the dependency relationship between

*Relationship between Tachigali's trunk diameters and distances to G. chlorogena's edifices. (a) Plotting distances to all the buildings associated with a given tree. (b) Plotting the average distance to the buildings associated* 

The nymphs spend several years underground, moving to reach the fine roots (less than 2 mm) from which they suck, with their rostrum, the elaborate sap on which they feed (see above). They move forward by digging galleries with their

On can consider [9] the beginning of the reproductive cycle at the time of mating (**Figure 19a**), after the nymph has emerged from its burrow and moulted into an imago (**Figure 19h, i**). The winged adults, stimulated by singing males, mate in trees. Then the females search for a stem in which they will plant their ovipositor several times [10] to deposit their eggs under the bark (**Figure 19b**). The larvae hatch on the twigs and then fall to the ground (**Figure 19c**) where they sink (**Figure 19d**). No one has yet observed their behaviour during this first phase of underground life. No one either knows the duration of the underground life until the exit to moult into a

From excavations undertaken after moulding with cement (see above), which revealed an inclination of the deepest zone of the well, as well as in its vicinity traces of oblique galleries of intermediate inclinations (**Figure 5b**), one can envisage the upwards digging of a vertical well from a deep horizontal gallery (**Figure 19e**) by digging successive oblique galleries more and more inclined

The digging of deep horizontal galleries giving access to fine roots that the nymphs can use to feed themselves (see above), is consistent with the presence of a

cicadas and their foster trees has to be explored in more detail.

forelegs, throwing the excavated material behind them.

winged imago; it is estimated at several years.

**9. Reproductive cycle**

**Figure 18.**

*with a given tree.*

**102**

(**Figure 19f**).

*Life cycle of G. chlorogena. (a) Mating. (b) Lay eggs. (c) After hatching, the tiny larvae (~ 2 mm) fall to the ground. (d) They bury themselves in the ground. (e) The nymph digs its gallery at the same time as it feeds on the sap of the roots. (f) As it moves forward and back, the nymph changes direction until it is vertically oriented. (g) The nymph digs the well which is a vertical gallery. (h) the turret is built from the well. (i) The nymph comes out of the turret to turn into an imago.*

significant biomass of fine roots in the deep soil layer of the Amazon rainforest, as recent research has shown [11]. The digging of successive oblique galleries more and more inclined implies a capacity of the nymph to back up into an already dug burrow. Such a capacity is observed when one surprises, by the withdrawal of its turret, a nymph near the exit of its well. It can also be observed in experiments where the nymph is placed in a glass tube.
