Introduction
⌅Tithonia diversifolia (Hemsl.) A. Gray., commonly known as Mexican sunflower, is a shrub species of the Asteraceae family with forage potential, which use in animal feeding is becoming increasingly important. Its agronomic performance (Londoño et al. 2019Londoño, C.J., Mahecha, L.L. & Angulo A.J. 2019. Desempeño agronómico y valor nutritivo de Tithonia diversifolia (Hemsl.) A Gray para la alimentación de bovinos. Revista Colombiana de Ciencia Animal - RECIA, 11(1): 1-10, ISSN: 2027-4297. https://doi.org/10.24188/recia.v0.n0.2019.693.), nutritional quality and value (Vargas et al. 2022Vargas, V.T., Pérez, P., López, S. & Castillo, E. 2022. Producción y calidad nutritiva de Tithonia diversifolia (Hemsl) A. Gray en tres épocas del año y su efecto en la preferencia por ovinos Pelibuey. Revista mexicana de Ciencias Pecuarias, 13(1): 240-257, ISSN: 2448-6698. https://doi.org/10.22319/rmcp.v13i1.5906.), rapid growth and low demand for inputs and management for its cultivation (Ríos 2002Ríos, C. 2002. Usos, manejos y producción de Botón de Oro, Tithonia diversifolia (Hemsl.) Gray. En: S. Ospina y E. Murgueitio (Eds.). Tres especies vegetales promisorias: Nacedero (Trichanthera gigantea (H &B) Nees.), Botón de Oro (Tithonia diversifolia (Hemsl.) Gray) y Bore (Alocasia macroohiza Linneo) Schott). Editorial CIPAV, Cali, Colombia. P. 211. ISBN: 9589386326.), together with its adaptability to multiple climates and soils, make it a strategic plant for the assembly of silvopastoral systems (SSP) (Murgueitio et al. 2015Murgueitio, E., Calle, Z., Xocchitl, M. & Uribe, F. 2015. Productividad en sistemas silvopastoriles intensivos en América Latina. En: F. Montagnini, E. Somarriba, E. Murgueitio, H. Fassola & B. Eibl (Eds.). Sistemas agroforestales, funciones productivas, socioeconómicas y ambientales. Editorial CIPAV, Cali, Colombia. pp 59-101. ISBN: 978-958-9386-74-3. and Murgueitio 2023Murgueitio, E. 2023. Tithonia diversifolia, a different Asteraceae: its function in sustainable systems of cattle production. Cuban Journal of Agricultural Science, 57, ISSN: 2079-3480. https://www.cjascience.com/index.php/CJAS/article/view/1090/1437.).
Comprehensive research, conducted at the Institute of Animal Science of Cuba, led by Ruiz et al. (2016)Ruiz, T.E., Alonso, J., Febles, G.J., Galindo, J.L., Savón, L.L., Chongo, B.B., Torres, V., Martínez, Y., La O, O., Gutiérrez, D., Crespo, G.J. Cino, D.M., Scull, I. & González, J. 2016. Tithonia diversifolia: I. Estudio integral de diferentes materiales para conocer su potencial de producción de biomasa y calidad nutritiva. Avances en Investigación Agropecuaria, 20(3): 63-82, ISSN: 0188-7890., confirm the benefits and attributes of this shrub for its use in animal production. As a result of these studies, T. diversifolia materials collected in Cuba are available, and can be used in grazing systems (Alonso et al. 2015Alonso J., Achang G., Santos, L.D.T. & Sampaiao R.A. 2015. Comportamiento productivo de Tithonia diversifolia en pastoreo con reposos diferentes en ambas épocas del año. Livestock Research for Rural Development, 27(6), ISSN: 0121-3784. http://www.lrrd.org/lrrd27/6/alon27115.html. and Ruiz et al. 2023aRuiz, T. E., J. Febles, G., Alonso, J., Torres, V., Valenciaga, N., Galindo, J., Mejías, R. & Medina, Y. 2023a. Comportamiento agronómico en pastoreo de materiales destacados de Tithonia diversifolia en Cuba. Avances en investigación Agropecuaria, 27(1): 136-145, ISSN: 0188-7890. https://doi.org/10.53897/RevAIA.23.27.26.). In this research, technological elements were defined for the use of this species in silvopastoral systems. Recently, it has been shown that its sowing by gamic seed can be sustained, with positive economic effects (Báez et al. 2022Báez, N., Padilla, C., Rodríguez García, I. & Ruiz, T.E. 2023. Análisis económico de la producción de semilla gámica de Tithonia diversifolia (Hemsl.) Gray en Cuba. Nota Técnica. Tropical Grasslands - Forrajes Tropicales, 11(1): 75-82, ISSN: 2346-3775. http://doi.org/10.17138/TGFT(11)75-82. and Padilla et al. 2023Padilla, C.R., Rodríguez, I.D., Ruiz, T.E., Báez, N., Medina, Y. & Herrera, M. 2023. Bases científico técnicas para la producción de semilla, siembra y establecimiento de Tithonia diversifolia (Hemsl.) A. Gray por vía gámica en Cuba. Anales Academia Ciencias de Cuba, 13(3): e1449, ISSN: 2304-0106. Available at: http://www.revistaccuba.cu/index.php/revacc/article/view/1449. ).
Despite there being few reports of damage or herbivory in this species, to achieve a deeper knowledge about phytosanitary, the objective of this study was to evaluate the entomofauna, associated with a silvopastoral system of T. diversifolia cv. ICA CUBA Oc-10, intended for bull fattening.
Materials and Methods
⌅Location
⌅The research was carried out for four years at the Institute of Animal Science (ICA), located at 22º 53' North, 82º 02' West, and 92 m a.s.l., in San José de las Lajas municipality, Mayabeque province, Republic of Cuba. The evaluation covered from 2019 to 2023.
Experimental area
⌅A total of 10 ha was used, which were composed of a mixture of improved grasses (Cynodon nlemfuensis) and natural grasses (Paspalum notatum, Sporobolus indicus, Dichantium sp.). The study area was divided into two systems, 5 ha each. One of them was composed of grasses (control area) and the other, of a silvopastoral system (SSP) of grasses-tithonia associated in 100 % of the area, which was intended for the fattening of male Siboney cattle from Cuba.
Tithonia SSP establishment methodology
⌅The sowing of T. diversifolia was carried out on a brown carbonated soil (Hernández et al. 2019Hernández, A., Pérez, J.M., Bosch, D. & Castro, N. 2019. La clasificación de los suelos de Cuba: énfasis en la versión de 2015. Cultivos Tropicales, 40(1): a15 - e15, ISSN: 1819-4087. Available at: http://ediciones.inca.edu.cu/index.php/ediciones/article/view/1504.), according to the concepts and methodologies developed by Ruiz and Febles (1999)Ruiz, T.E. & Febles, G. 1999. Sistemas silvopastoriles. Conceptos y tecnologías desarrollados en el Instituto de Ciencia Animal de Cuba. EDICA. Instituto de Ciencia Animal. La Habana. Cuba. pp. 43. and Ruiz et al. (2006)Ruiz, T.E., Febles, G., Jordán. J., Castillo, E., Mejías R., Crespo, G., Chongo, B., Delgado, D., Alfonso, H., Escobar, A. & Ramírez. R. 2006. Conceptos y Tecnologías desarrolladas en el Instituto de Ciencia Animal. En: Fisiología. Producción de biomasa y sistemas silvopastoriles en pastos tropicales. Abono orgánico y biogás. Tomo II. Edición EDICA. Cuba. 136 p.. Previous soil preparation was carried out in strips in grassland areas. The tithonia strips were oriented from East to West and sowing was performed by cuttings, pastures and botanical seed. For this, the registered variety ICACUBA Oc-10 was used, proposed by Ruiz et al. (2010)Ruiz, T.E., Febles, G., Torres, V., González, J., Achang, G., Sarduy, L. & Díaz, H. 2010. Evaluación de materiales recolectados de Tithonia diversifolia (Hemsl.) Gray en la zona centro-occidental de Cuba. Revista Cubana de Ciencia Agrícola, 44(3): 291-296, ISSN: 0034-7485. for its implementation in grazing.
Experimental procedure
⌅For studies of the associated entomofauna, the baseline was initially drawn in both areas before sowing tithonia. Two samples of 20 raids were taken in an area representative of the area to be sown, and two equal samples in the control area, composed by grasses. Subsequently, with the promotion of the SSP, stratified sampling was implemented in five blocks. In the center of each block, the representative sampling area was defined, according to the methodology proposed by CIBA-GEIGY (1981)CIBA-GEISY 1981. Manual para ensayos de campo en protección vegetal. Segunda edic. revisada y ampliada. Werner Püntener, División Agricultura. Switzerland. 205 p.. Sampling was carried out at three climatic times of the year (January, May and September). In each block, a sample of 20 raids was taken with the use of the entomological network for each plant component (tithonia and base grass) for a total of 10 samples (five in tithonia and five in the base grass). In the control area, established only with grasses, five samples were taken. All were individualized in plastic bags, with their respective identifications, and were transferred to the Pest Management Laboratory of the Pasture Department of the ICA for their processing and taxonomic identification. A stereoscopic microscope, entomological collections and related dichotomous keys were used for this purpose. Phytophagous insects, visiting organisms and the associated beneficial fauna (bioregulators) were identified in each study area, considering the assignment of functional groups, according to Metcalf and Flint (1965)Metcalf, C.L. & Flint, W.P. 1965. Insectos destructivos e insectos útiles: sus costumbres y su control. Instituto Cubano del Libro. La Habana, Cuba, 1208 p., Triplehorn and Johnson (2005)Triplehorn C.A. & Johnson N.F. 2005. Borror and DeLong's lntroduction to the Study of lnsects. Thomson Brooks/Cole, USA, 864 p., Seventh Edition, ISBN 003-096835-6. https://www.academia.edu/30669150/Borror_and_Delong_2005_Study_of_Insects., Mancina and Cruz (2017)Mancina, C.A. & Cruz, D.D. 2017. Diversidad biológica de Cuba: métodos de inventario, monitoreo y colecciones biológicas. Editorial AMA, La Habana, 480 p. ISBN: 978-959-300-130-4 (versión digital). and World Spider Catalog (2020)World Spider Catalog 2020. World Spider Catalog. Version 21.5. Natural History Museum Bern. https://doi.org/10.24436/2. Available at: http://wsc.nmbe.ch. . The level of damage caused by insect-pests in each plant component was also evaluated, in accordance with what was described by Calderón (1982)Calderón, M. 1982. Evaluación del daño causado por insectos. En: J. M. Toledo (Ed.). Manual para la Evaluación Agronómica. CIAT, Red Internacional de Evaluación de Pastos Tropicales. Cali, Colombia. p. 80..
Climatic conditions of the study area
⌅Average annual temperature was 24.86 °C. The accumulated rainfall in 2019 was 1,254.7 mm, with 71 days of rain. In 2020, there was an accumulated of 1,599.4 mm in 118 days. In January, May and September, it was 6.9 mm with 4 d of rain, 351.8 mm with 13 d and 240.7 mm with 15 d, respectively. The accumulated rainfall in 2021 was 1,497.9 mm with 88 days of rain. January had 34 mm in just 1 day, May only 40.1 mm with 7 days and September 218.7 mm with 15 days. In 2022, the accumulated rainfall was 1,903.7 mm within 100 days. In January, May and September, 24.9 mm, 253.8 mm and 258.1 mm were registered in 4 d, 14 d and 18 d, respectively. In 2023, it was 1,171.6 mm in 95 days of rain: January with 4.6 mm in 2 days, May with 182.5 mm in 13 days and September with 159.8 mm in 12 days of rain. This last year appeared to have more rain. However, the accumulated rainfall was much lower than the historical mean (40 years), with 258.4 mm less. On the contrary, in 2022, it rained 473.7 mm more than the historical mean.
Data processing and analysis
⌅An Excel database was created with all the collected information. The ecological indicators were determined: number of individuals (N), species richness (S), uniformity (E), Margalef index (DMg), Simpson index (Dsp), Shannon index (H'), Shannon variance, Berger-Parker index (d) and alpha (log distribution) for the baseline, according to the Diversity program, according to Henderson and Seaby (1998)Henderson, P.A. & Seaby, R.M.H. 1998. Species diversity & Richness. Version 2.2. Pisces Conservation. Ltd, IRC, House, Pennintong, Lymintong, UK.. Then, the associated arthropodfauna was grouped in each experimental area according to the plant component and the richness and abundance of species, according to the sampling moment in the year. In the first year, proportion comparison analysis (chi-square) was carried out for each plant component evaluated, according to the ComparPro version 1 statistical package (Font et al. 2007Font, H., Noda, A., Torres, V., Herrera, M., Lizazo, D., Sarduy, L. & Rodríguez, L. 2007. Paquete estadístico ComparPro versión 1. Instituto de Ciencia Animal, Dpto Biomatemática. ). For the abundance of species, the procedure was performed according to the sampling moment and the test of Duncan (1955)Duncan, D.B. 1955. Multiple Range and Multiple F Tests. Biometrics, 11(1): 1-42, ISSN: 0006-341X. https://doi.org/10.2307/3001478. for P<0.05 was applied to differentiate means in the necessary cases.
In the second year of sampling, relative frequency (Fr) and relative abundance (Ar) of the associated arthropodfauna were determined, with emphasis on the insect fauna. In addition, the percentage of intensity (% intensity) and of distribution (% distribution) were determined when moderate insect lesions were found. Next, the corresponding formulas and scales are issued according to INISAV (2006)INISAV 2006. Resumen. Metodología de señalización y pronósticos. La Habana.:
where:
Fr: relative frequency
Fi: times in which each insect appeared per month
Ft: number of times it was evaluated
Scale
where:
Ar: relative abundance
n: number of individuals of one species per month
N: total number of all the collected individuals from the different species found
where:
n: # of studied leaves
N: total # of studied leaves
i: highest value of the scale
v: value of the scale (1 to 4)
where:
a: number of affected leaves
b: number of sampled leaves
Results and Discussion
⌅Table 1 shows the ecological indicators recorded in the baseline carried out before the promotion of the SSP. Homogeneity is demonstrated in both areas, as there is no evidence of dominant species (0.3217 and 0.2692). As can be seen, there was similarity in the range of abundance (136 and 153), as well as in uniformity (0.7197 and 0.8411) for the area to be sown and the control area, respectively. This is demonstrated by the Diversity program (Henderson and Seaby 1998Henderson, P.A. & Seaby, R.M.H. 1998. Species diversity & Richness. Version 2.2. Pisces Conservation. Ltd, IRC, House, Pennintong, Lymintong, UK.), when graphing the range of abundance of the collected species (figure 1).
| Diversity index | Sowing area | Control |
|---|---|---|
| Number of individuals (N) | 136 | 153 |
| Species richness (S) | 14 | 23 |
| Uniformity (E) | 0.7197 | 0.8411 |
| Margalef index (DMg) | 2.7398 | 4.3566 |
| Simpson index (Dsp) | 6.9439 | 9.4159 |
| Shannon index (H’) | 2.2566 | 2.6374 |
| Shannon variance | 0.0075 | 0.0068 |
| Berger-Parker index (d) | 0.3217 | 0.2692 |
| Alpha (log distribution) | 4.1761 | 7.4441 |
The taxonomic identification of the arthropodfauna associated with the SSP with tithonia and base grass, as well as in the control area, only with grasses (C. nlemfuensis + natural grasses) showed that Insecta class has superiority with respect to the rest (Malacostroca, Gastropoda and Arachnida). This result is evident, knowing that insects can indeed be found in almost all environments on the planet and are considered as the most diverse group of animals on Earth, with approximately one million described species. More than all other groups of animals combined, it is estimated that there could be up to 10 million species of insects not yet described (Barrera and López 2016Barrera, L. & López, P. 2016. Naturaka Planeta insecto. NaturalMente, 10. Available at: https://www.mncn.csic.es/es/Comunicaci%C3%B3n/naturaka-planeta-insecto. ). During the experimental period, 14 orders, 37 families and 76 morphospecies were collected (table 2). In total, 38 morphospecies with phytophagous habits, 13 visitors, 22 bioregulatory morphospecies, 2 hematophagous and 1 omnivorous were associated.
| CLASS | ORDER | FAMILY | SCIENTIFIC NAME | COMMON NAME | FUNCTIONAL GROUP |
|---|---|---|---|---|---|
| Insecta | Hemiptera | Cicadellidae | Empoasca sp. δ ϕ £ | Leafhopper | F |
| Hortensia similis (Walk.) δ ϕ £ | Leafhopper | F | |||
| Draeculacephala cubana (M y B.) ϕ £ | Leafhopper | F | |||
| Chlorotettix minimus Baker δ ϕ £ | Leafhopper | F | |||
| Thamnotettix sp. δ ϕ £ | Leafhopper | F | |||
| - | 2 unidentified morphospecies £ | Leafhoppers | F | ||
| Flatidae | Ormenaria rufifascia (Walker) £ | Palm flatid planthopper | F | ||
| Cixiidae | Bothriocera sp. δ ϕ £ | Cixiid | F | ||
| Oliarus sp. δ ϕ £ | Cixiid | F | |||
| Membracidae | Stictocephala rotundata Stål. ϕ £ | treehopper | F | ||
| Rhyparochromidae | Paromius longulus (Dallas) ϕ £ | Long grey seed bug | F | ||
| Pentatomidae | Mormidea pictiventris (Stål) ϕ £ | Stink bug | F | ||
| Nezara viridula L. ϕ £ | Green stink bug | F | |||
| - | 1 unidentified morphospecie ϕ £ | Stink bug | F | ||
| Diptera | Dolichopodidae | Condylostylus sp. δ ϕ £ | Fly | B | |
| Chamaemyiidae | Leucopis sp. δ ϕ £ | Fly | V | ||
| Otitidae | Euxesta stigmatias (Loew.) δ ϕ £ | Cornsilk fly | V | ||
| Syrphidae | Toxomerus sp. δ ϕ £ | Syrphid fly | B | ||
| Culicidae | Culex pipiens L. £ | mosquito | H | ||
| - | 5 unidentified morphospecies δ ϕ £ | dipteran | V | ||
| Lepidoptera | Crambidae | Omiodes (Hedylepta) indicata (Fab.) δ | Bean-leaf webworm moth | F | |
| - | 4 unidentified morphospecies δ | Butterflies | V | ||
| Noctuidae | 3 unidentified morphospecies δ | Moths | F | ||
| 1 unidentified morphospecie ϕ £ | Lepidopteran larvae | F | |||
| Coleoptera | Chrysomelidae | Diabrotica sp. δ ϕ £ | Cucurbit beetle | F | |
| Colaspis brunnea (Fab.) ϕ £ | Leaf beetle | F | |||
| Deloyala guttata (Oliver) δ ϕ £ | Mottled tortoise beetle | F | |||
| Oedionychus pictus (Fab.) ϕ £ | beetle | F | |||
| Diachus auratus (Fab.) δ ϕ £ | Bronze leaf beetle | F | |||
| Epitrix sp. δ ϕ £ | Flea beetle | F | |||
| Typophorus nigritus F. δ ϕ | Sweetpotato leaf beetle | F | |||
| Cryptocephalus viridipennis Suffrian δ ϕ | Leaf beetle | F | |||
| Anisostena cyanoptera Suffrian δ ϕ | Leaf beetle | F | |||
| Curculionidae | Centrinaspis sp. ϕ | Leaf beetle | F | ||
| Coccinellidae | Brachiacantha bistripustulata Fab. δ ϕ | Ladybug | B | ||
| Chilocorus cacti Lδ ϕ | Ladybug | B | |||
| Cycloneda sanguinea limbifer Casey δ ϕ | Ladybug | B | |||
| Lycidae | Thonalmus suavis Duval ϕ | Net-winged beetle | F | ||
| - | 1 unidentified morphospecie ϕ | Little black beetle | F | ||
| Hymenoptera | Apididae | Apis mellifera L. δ | Bees | V | |
| Ichneumonidae | Ophion sp. δ ϕ £ | Ichneumonid wasp | B | ||
| Coccygomimus rufoniger (Cresson) δ | Wasp | B | |||
| Chalcididae | Brachymeria robusta Alayo y Hernández δ | Chalcid wasp | B | ||
| Conura (Spilochalcis) femorata Fab. δ | Chalcid wasp | B | |||
| 2 unidentified morphospecies δ | Chalcid wasp | B | |||
| Formicidae | Wasmannia auropunctata (L.) δ ϕ £ | Little fire ants | B | ||
| Paratrechina longicornis Latreille δ ϕ £ | Crazy ant | V | |||
| Vespidae | 2 unidentified morphospecies δ | Wasps | B | ||
| Orthoptera | Tettigonidae | Conocephalus cuspidatus (Scud.) ϕ £ | Long-horned grasshopper | F | |
| Conocephalus sp. ϕ £ | Conehead | F | |||
| - | 1 unidentified morphospecie ϕ £ | Grasshopper | F | ||
| Neuroptera | Chrysopidae | Chrysopa sp. δ | Green lacewing | B | |
| Dermaptera | Forficulidae | Doru taeniatum (Dohr.) δ | Earwig | B | |
| Thysanoptera | Thripidae | 1 unidentified morphospecie ϕ £ | Trip | F | |
| Blattodea | Blattidae | Periplaneta americana L. ϕ £ | Cockroach | O | |
| Malacostraca | Isopoda | Armadillidae | Armadillidium vulgare (Latreille) ϕ £ | Common pill woodlouse | F |
| Gastropoda | - | - | 1 unidentified morphospecie δ ϕ £ | Snail | F |
| Arachnida | Araneae | - | 6 unidentified morphospecies δ ϕ £ | Spiders | B |
| Ixodida | Ixodidae | Rhipicephalus (Boophilus) microplus Canestrini δ ϕ £ | Ticks | H |
V- visitors F- phytophagous B- bioregulators H-hematophagous O- omnivores δ SSP-tithonia ϕ SSP-pasto £ control (grasses)
With the exception of visiting organisms, mainly associated with the flowering season, attracted by the tithonia flowers, such as bees (Apis mellifera), butterflies and dragonflies, the rest frequent the plant component of the areas (SSP with tithonia, SSP base grass and control grass), in greater or lesser proportion, at some time of the year.
Among the most recurring phytophages, a complex group of leafhoppers (Empoasca sp., Hortensia similis, Draeculacephala cubana) and another of chrysomelids of Epitrix, Diabrotica, Colaspis, Diachus, Typophorus, Cryptocephalus, Oedionychus and Anysostena genera were found, which, although were observed in tithonia, exert their damage with greater emphasis on base grass and grasses (control area). It was confirmed that only the bean-leaf webworm moth (Omiodes indicata) prefers tithonia, where it develops its entire biological cycle. However, T. diversifolia is still a plant that pests consume little, with a low damage percentage, inferior to 20 %. This result coincides with what was reported in studies by Ruiz et al. (2017)Ruiz, T.E., Febles, G.J., Alonso, J., Crespo, G. & Valenciaga, N. 2017. Chapter X. Agronomy of Tithonia diversifolia in Latin America and the Caribbean región. pp. 171-201. In: L. L. Savón Valdes, O. Gutierrez Borroto & G. Febles Pérez (Eds.) Mulberry, moringa and Tithonia in animal feed, and other uses. Results in Latin America and the Caribbean. FAO. ICA-EDICA, Cuba. ISBN: 978-959-7171-72-0. Available at: https://www.feedipedia.org/sites/default/files/public/savonvaldes_2017.pdf. under Cuban conditions. This performance could be associated with the presence of secondary metabolites in the plant (Scull et al. 2022Scull, I., Savón, L.L., Ruiz, T. E. & Herrera, M. 2022. Effect of growth age on the polyphenol content of materials from Tithonia diversifolia (Hemsl.). Cuban Journal Agricultural Science, 56(3): 209-217, ISSN: 2079-3488. Available at: http://scielo.sld.cu/pdf/cjas/v56n3/2079-3480-cjas-56-03-e04.pdf. ).
González-Sierra et al. (2019)González-Sierra, L., Díaz-Solares, M., Castro-Cabrera, I., Fonte-Carballo, L., Lugo-Morales. Y. & Altunaga-Pérez. N. 2019. Caracterización fitoquímica y actividad antioxidante total de diferentes extractos de Tithonia diversifolia (Hemsl) A. Gray. Pastos y Forrajes, 42(3): 243-248, ISSN: 2078-8452. Available at: <https://payfo.ihatuey.cu/index.php?journal=pasto&page=article&op=view&path%5B%5D=2147>. , when carrying out the qualitative and quantitative determination of said metabolites in ethanolic extracts of roots, stems and leaves of T. diversifolia under the conditions of Cuba, reported a wide variety of bioactive substances like phenols, flavonoids, coumarins, quinones and terpenoids, with higher contents in roots and with great antioxidant activity.
In a similar study by Sabaris et al. (2023)Sabaris, S.B., Sadiq, M., Karanath-Anilkumar, A., Sireesha, R. & Munuswamy-Ramanujam, G. 2023. Comparative bioactivity evaluation of secondary metabolites from the leaves, stem and flowers of Tithonia diversifolia. Materials Today: Proceedings, Volume 93. Part 2. Pages 28-39. ISSN: 2214-7853. https://doi.org/10.1016/j.matpr.2023.09.042. multiple bioactive substances were found present in leaves, stems and flowers, which are used by the plant as a defense mechanism after the action of herbivores. Hence, they are capable of manifesting repellent, phagodeterrent or insecticidal action against certain pest-insects (Bagnarello et al. 2009Bagnarello, G., Hilje, L., Bagnarello, V., Cartin, V. & Calvo, M. 2009. Actividad fagodisuasiva de las plantas Tithonia diversifolia y Montanoa hibiscifolia (Asteraceae) sobre adultos del insecto plaga Bemisia tabaci (Homoptera: Aleyrodidae). Revista Biología Tropical, 57(4): 1201-1215, ISSN: 0034-7744., Castaño-Quintana et al. 2013Castaño-Quintana, K., Montoya-Lerma, J. & Giraldo-Echeverri, C. 2013. Toxicity of foliage extracts of Tithonia diversifolia (asteraceae) on Atta cephalotes (Hymenoptera: Myrmicinae) workers. Industrial Crops and Products, 44: 391-395, ISSN: 1872-633X. https://doi.org/10.1016/j.indcrop.2012.11.039., Rodríguez et al. 2015Rodríguez, J., Montoya-Lerma, J. & Calle, Z. 2015. Effect of Tithonia diversifolia Mulch on Atta cephalotes (Hymenoptera: Formicidae) Nests. Journal of Insect Science, 15(1): 32-38, ISSN: 1536-2442. https://doi.org/10.1093/jisesa/iev015., Jiménez et al. 2016Jiménez, L., Arias, A., Valdés, R. & Cárdenas, M. 2016. Tithonia diversifolia, Moringa oleifera y Piper auritum: Alternativas para el control de Sitophilus oryzae. Centro Agrícola, 43(3): 56-62, ISSN: 2072-2001. Available at: http://cagricola.uclv.edu.cu. , Devi et al. 2022Devi, T.B., Raina, V. & Rajashekar, Y. 2022. A novel biofumigant from Tithonia diversifolia (Hemsl.) A. Gray for control of stored grain insect pests. Pesticide Biochemistry and Physiology, 184: 105-116, ISSN: 0048-3575. https://doi.org/10.1016/j.pestbp.2022.105116., Kerebba et al. 2022Kerebba, N., Oyedeji, A.O., Byamukama, R., Kuria, S.K. & Oyedeji, O.O. 2022. Evaluation for Feeding Deterrents Against Sitophilus zeamais (Motsch.) from Tithonia diversifolia (Hemsl.) A. Gray. Journal of Biologically Active Products from Nature, 12(1): 77 - 93, ISSN: 2231-1874. https://doi.org/10.1080/22311866.2021.2023046. and Miranda et al. 2022Miranda, M.A.F.M., Matos, A.P., Volante, A.C., Cunha, G.O.S. & Gualtieri, S.C.J. 2022. Insecticidal activity from leaves and sesquiterpene lactones of Tithonia diversifolia (Helms.) A. Gray (Asteraceae) on Spodoptera frugiperda (Lepidoptera: Noctuidae). South African Journal of Botany, 144(1): 377-379, ISSN: 0254-6299. https://doi.org/10.1016/j.sajb.2021.09.002.). Its molluscicide action has even been recently verified from foliar extracts of the plant (Ballada and Baonan 2023Ballada, K.A. & Baoanan, Z.G. 2023. Molluscicidal properties of wild sunflower (Tithonia diversifolia) leaf extract fractions against invasive golden apple snail (Pomacea canaliculata) . Environment, Development and Sustainability, 25(10), ISSN: 1573-2975. https://doi.org/10.1007/s10668-023-03969-5.).
Other studies report that the plant has allelopathic action (Tongma et al. 2001Tongma S, Kobayashi K & Usui K. 2001. Allelopathic activity of Mexican sunflower [Tithonia diversifolia (Hemsl.) A. Gray] in soil under natural field conditions and different moisture conditions. Weed Biology and Management, 1(2): 115-119, ISSN: 1445-6664. https://doi.org/10.1046/j.1445-6664.2001.00020.x., Rodríguez-Cala and González-Oliva 2017Rodríguez-Cala, D. & González-Oliva L. 2017. Testing the allelopathic effect of Tithonia diversifolia (Asteraceae) on a model species. Acta Botánica Cubana, 216: 167-174, ISSN: 2519-7724. Available at: http://repositorio.geotech.cu/xmlui/bitstream/handle/1234/1462/Testing%20the%20allelopathic%20effect%20of%20Tithonia%20diversifolia%20%28Asteraceae%29%20on%20a%20model%20species.pdf?sequence=1&isAllowed=y. ), nematocidal (Ferreira et al. 2012Ferreira, I.C.M., Silva, G.S. & Nascimento, F.S. 2013. Efeito de extratos aquosos de espécies de Asteraceae sobre Meloidogyne incognita Summa Phytopathologica. Botucatu, 39(1): 40-44, ISSN: 1807-5762. https://doi.org/10.1590/S0100-54052013000100007. and Neto et al. 2018Alcântara Neto, F.D.A., Delpupo, K.C., da Silva, G.S., Gravina, G.D.A., de Melo, M.P. & Beserra-Júnior, J.E.A. 2018. Folhas de girasol mexicano como alternativa no manejo de Pratylenchus brachyurus em quiabeiro. Summa Phytopathologica, 44(3): 267-270, ISSN: 1980-5454. https://doi.org/10.1590/0100-5405/169428. ), as well as anthelmintic action (Duarte et al. 2020Duarte, E.R., David, P.P.D., Oliveira, K.B.A., de Lima, M.D., Magaço, F.D.S. & Morais-Costa, F. 2020. Efficacy of Tithonia diversifolia (Hemsl) A. Gray on the inhibition of larval development of Haemonchus contortus. Acta Veterinaria Brasilica, 14(3): 191-195, ISSN: 1981-5484. Available at: https://periodicos.ufersa.edu.br/index.php/acta/index.) and antiparasitic (Lezcano-Más et al. 2016Lezcano-Más, Y., Soca-Pérez, M., Roque-López, E., Ojeda-García, F., Machado-Castro, R. & Fontes-Marrero, D. 2016. Forraje de Tithonia diversifolia para el control de estrongílidos gastrointestinales en bovinos jóvenes. Pastos y Forrajes, 39(2): 133-138, ISSN: 2078-8452. Available at: https://payfo.ihatuey.cu/index.php?journal=pasto&page=article&op=view&path%5B%5D=1893&path%5B%5D=2739. ). This ability of the plant to maintain a low incidence of pest-causing organisms and, consequently, low damage levels, constitutes a novel result, obtained and verified in the present study, which enhances the interest in its use, which makes it even more attractive to encourage its use in animal feeding.
The control area, with only grasses, always obtained the highest abundances at the time of sampling with respect to the rest of the evaluated plant components (table 3). Studies by Alonso-Amaro et al. (2021)Alonso-Amaro, O., Fernández-García, I., Lezcano-Fleires, J.C. & Suris-Campos, M. 2021. Diversidad entomofaunística funcional en una asociación de árbol forrajero-pasto en el contexto ganadero cubano. Pastos y Forrajes, 44: eE30, ISSN: 2078-8452. http://scielo.sld.cu/pdf/pyf/v44/2078-8452-pyf-44-e30.pdf. in leucaena-guinea silvopastoral systems also obtained higher values of insect diversity, numerous and similar in the sampled areas, although not representative for the herbaceous stratum.
| Plant component | Sampling moment | Orders | Species richness | Abundance | Percentage |
|---|---|---|---|---|---|
| SSP tithonia | January | 6 | 15 | 221 | 52.49a |
| May | 7 | 15 | 86 | 20.42c | |
| September | 7 | 16 | 114 | 27.07b | |
| SE and Signif. | ±2.29 P<0.001 | ||||
| Total | 421 | 100 | |||
| SSP base grass | January | 9 | 24 | 237 | 29.81b |
| May | 8 | 38 | 196 | 24.65c | |
| September | 8 | 28 | 362 | 45.53a | |
| SE and Signif. | ±1.67 P<0.001 | ||||
| Total | 795 | 100 | |||
| Control (grass) | January | 8 | 24 | 274 | 20.01b |
| May | 9 | 29 | 215 | 15.70c | |
| September | 8 | 34 | 880◆ | 64.28a | |
| SE and Signif. | ±1.27 P<0.001 | ||||
| Total | 1,369 | 100 | |||
a,b,c- Common letters in each plant component are not significantly different (p<0.05) (Duncan 1955Duncan, D.B. 1955. Multiple Range and Multiple F Tests. Biometrics, 11(1): 1-42, ISSN: 0006-341X. https://doi.org/10.2307/3001478. )
♦- 530 species of Hortensia similis leafhopper in 880 total individuals
May was also the month with the lowest proportion of insects, collecting the lowest abundances with significant differences with the rest. This could be due to the fact that it was the month when the dry period intensified (40.1 mm) and, logically, the plant species were also suffering from the lack of water in the soil. Therefore, the plants are less turgid and less desirable by the phytophagous organisms that feed on them. This performance has been evident in multiple studies, where climatic factors determine the appearance of organisms associated with plants (Baltazar 2016Baltazar, H. 2016. Factores climáticos que influyen en la diversidad de insectos en Spartium junceum L. (Fabales: Fabaceae). Prospectiva Universitaria Depósito Legal en la Biblioteca Nacional del Perú, N° 2006-4116 p - ISSN: 1190-2409 / e- ISSN 1990 - 7044 Vol. N° 13. Números 1 y 2. pp. 30-48. and Doria-Bolaños et al. 2021Doria-Bolaños, M., García-Gonzales, P. & Fachin-Ruiz, G. 2021. Estudio de diversidad de la entomofauna en el Centro de Biodiversidad de la Universidad Nacional de San Martín. Revista Agrotecnológica Amazónica, 1(2): 15-26, ISSN: 2710-0510. https://doi.org/10.51252/raa.v1i2.177.), and even more so if it is known, according to research by Herrera et al. (2018)Herrera, R.S., García, M. & Cruz, A.M. 2018. Study of some climate indicators at the Institute of Animal Science from 1967 to 2013 and their relation with grasses. Cuban Journal of Agricultural Science, 52(4): 411-421, ISSN: 2079-3480. https://www.cjascience.com/index.php/CJAS/article/view/831/827. , the evident effect of climate change in the study area. Insects, due to their very short life cycles (days, weeks), compared to other animals or plants, can have effects on their development, movement, reproduction and performance in front of these extreme climatic episodes, such as heat waves or temperature variations (Nolasco et al. 2021Nolasco, J., Sánchez, R.A., Villalobos, F. & González, D. 2021. Los insectos ante el cambio climático. Instituto de Ecología (INECOL), México. Available at: https://www.inecol.mx/inecol/index.php/es/ct-menu-item-25/ct-menu-item-27/17-ciencia-hoy/1497-los-insectos-ante-el-cambio-climatico.). In this way, younger leaves are consumed more by herbivores, since they represent a more nutritious resource and, presumably, are not so defended by chemical substances, especially by compounds that reduce their digestibility and, therefore, herbivores prefer them to old leaves with greater resistance due to the accumulation of structural compounds (Rusman et al. 2020Rusman, Q., Lucas-Barbosa, D., Hassan, K. & Poelman, E.H. 2020. Plant ontogeny determines strength and associated plant fitness consequences of plant mediated interactions between herbivores and flower visitors. Journal of Ecology, 108(3): 1046-1060, ISSN: 1365-2745. https://doi.org/10.1111/1365-2745.13370.). However, recent research carried out in Yucatán, Mexico, by Ruiz-Santiago et al. (2023)Ruiz-Santiago, R.R., Ballina-Gómez, H.S. & Ruiz-Sánchez, E. 2023. Características morfológicas foliares y su relación con la defoliación en tres especies de plantas forrajeras. Acta Biológica Colombiana, 28(1): 12-22, ISSN: 1900-1649. https://doi.org/10.15446/abc.v28n1.88402. evaluated the influence of plant and leaf age on foliar characteristics and its relationship with defoliation caused by herbivorous insects in three forage species (Tithonia diversifolia, Morus alba and Moringa oleifera). Results showed that there is more defoliation in old and intermediate leaves compared to young leaves in T. diversifolia. In relation to age, defoliation was significant in plants with 60 d. Studies by Ambrósio et al. (2008)Ambrósio, S.R., Oki, Y., Heleno, V.C.G., Chaves, J.S., Nascimento, P.G.B.D., Lichston, J.E., Constantino, M.G., Varanda, E.M. & Da Costa, F.B. 2008. Constituents of glandular trichomes of Tithonia diversifolia: Relationships to herbivory and antifeedant activity. Phytochemistry, 69(10): 2052-2060, ISSN: 0031-9422. https://doi.org/10.1016/j.phytochem.2008.03.019. attribute the relationship between herbivory and the antifeedant activity manifested by Tithonia diversifolia to the presence of trichomes on its leaves with a high load of secondary metabolites, which prevents its action by exerting antimicrobial defense.
A strong attack of leafhoppers occurred in this control area in September, in which the climatic conditions were favorable for its appearance with dominance of Hortensia similis. Out of the 880 total collected insects, 530 corresponded to this specimen alone, associated with the prairie grasses present in said area (star grass and natural grasses). However, these high population levels of phytophagous insects, with a biting-sucking habit, were not frequent over time, and it is possible that the presence of the beneficial fauna associated with SSPs has also prevented populations from increasing and economic damages.
Studies by Ramírez-Barajas et al. (2019)Ramírez-Barajas, P.J., Santos-Chable, B.E., Casanova-Lugo, F., Lara-Pérez, L.A., Tucuch-Haas, J.I., Escobedo-Cabrera, A., Villanueva-López, G. & Díaz-Echeverría, V.F. 2019. Diversidad de macro-invertebrados en sistemas silvopastoriles del sur de Quintana Roo, México. Revista de Biología Tropical, 67(6): 1383-1393, ISSN: 0034-7744. Available at: https://www.scielo.sa.cr/pdf/rbt/v67n6/0034-7744-rbt-67-06-1383.pdf. highlighted the role of trees and shrubs in creating these refuge sites, microclimates and suitable habitats so that a greater number of organisms, such as insects, can coexist. However, many other groups of living beings can also coexist in functional biodiversity: birds, reptiles, mammals, amphibians and mollusks, which, together with the presence of cattle, which constitute the main animal component in the SSP, actively participate in the agroforestry dynamics. That is why these systems are granted greater connectivity with natural ecosystems with respect to conventional ones with single-crop pastures, which in turn suggests ideas for the integration between livestock production and biodiversity conservation (Harvey et al. 2004Harvey, C.A., Tucker, N.I.J. & Estrada, A. 2004. Live fences, isolated trees, and windbreaks: tools for conserving biodiversity in fragment tropical landscape. In: G. Schroth, G.A.B. da Fonseca, C.A. Harvey, C. Gascon, H.L. Vasconcelos & A.M.N. Izac (Eds.) Agroforestry and biodiversity conservation in tropical landscapes. Washington: Island Press. p.261-289. https://www.researchgate.net/publication/325128589_Live_Fences_Isolated_Trees_and_Windbreaks_Tools_for_Conserving_Biodiversity_in_Fragmented_Tropical_Landscapes. ). Something similar occurs with agroecosystems composed of polycultures (García-González et al. 2022García González, M.T., Rodríguez Coca, L.I., Fernández Cancio, Y., Rodríguez Jáuregui, M.M. & Gil Unday, Z. 2022. Biodiversidad de insectos en sistemas de policultivos de maíz (Zea mays L.). Ecosistemas, 31(3): 2400-2405, ISSN: 1697-2473. https://doi.org/10.7818/ECOS.2400.), which host greater diversity of insects with higher proportions of beneficial fauna. Studies by Ruiz et al. (2023b)Ruiz, T.E., Febles, G.J., Alonso, J. & Valenciaga, N. 2023b. El árbol y su efecto en la estabilidad productiva vegetal en un Sistema Silvopastoril. pp. 54-57. En: Rivera J., Viñoles C., Fedrigo J., Bussoni A., Peri P., Colcombet L., Murgueitio E., Quadrelli A. & Chará J. (Eds.) Sistemas Silvopastoriles: Hacia una Diversificación Sostenible. CIPAV. Cali, Colombia. ISBN 978-628-95190-5-1. highlighted the importance of the tree component in the benefits provided by the silvopastoral system.
The insects collected in the experimental area during the evaluated period, which reached the category of frequent, according to the used scale (≥ 10 ≤ 29), were from the orders Hemiptera (Empoasca sp., Hortensia similis and Draeculacephala cubana), Diptera (two unidentified morphospecies), Orthoptera (Caulopsis cuspidatus) and the order Hymenoptera (Paratrechina longicornis and Wasmannia auropunctata). The order Araneae (two unidentified morphospecies) also stood out from the class Arachnida. The rest of the collected specimens were in the low frequent range (< 10). None reached the category of very frequent. Even in this period, the leaf pecker (Omiodes indicata) could be seen, which, although it has been recorded with a preference for protein crops (Valenciaga et al. 2018Valenciaga, N., Ruiz, T.E., Mora, C.A. & Díaz, H. 2018. Evaluación fitosanitaria de 24 materiales de Tithonia diversifolia (Hemsl.) Gray recolectados en la región oriental de Cuba. Memoria del VI Congreso PAT 2018. CD-ROM. La Habana. ISBN: 9789-959-7171-80-5.), population levels in this study were minimal. Therefore, the lesions found did not exceed slight damage, so their intensity and distribution were not determined, as there was no economic damage to the crop.
In the silvopastoral system, Tithonia diversifolia remains as plant tolerant to the attack of harmful organisms. In this period, practically no presence or incidence of the chrysomelid complex was observed. Only Colaspis brunnea and Deloyola guttata were little frequent, both collected in the base pasture. In January, the cattle tick Rhipicephalus (Boophilus) microplus appeared, although with low frequency, and mainly associated with grass, in the base pasture of the SSP as in the control area. R. microplus is known to be a single-host tick, which spends all of its life stages on the same animal, sucking blood. The female of this organism in its adult phase falls to the ground where it lays eggs. Therefore, the eggs are said to hatch in the environment and the newly hatched larvae crawl across grass or other plants to find a host (CFSPH 2007CFSPH (The Center for Food Security & Public Health) 2007. Rhipicephalus (Boophilus) microplus Garrapata del ganado del sur, garrapata del ganado bovino. Ioawa State University. College of Veterinary Medicine. Available at: https://www.cfsph.iastate.edu/Factsheets/es/boophilus_microplus-es.pdf. , Alonso-Díaz and Fernández-Salas 2022Alonso-Díaz, M.A. & Fernández-Salas, A. 2022. Rhipicephalus microplus: biología, control y resistencia. Centro de Enseñanza, Investigación y Extensión en Ganadería Tropical de la Facultad de Medicina Veterinaria y Zootecnia UNAM, México. 40 p. Available at: https://www.fmvz.unam.mx/fmvz/centros/ceiegt/archivos/Manual_R_Microplus.pdf. ). This justifies finding tick larvae or first instars in the collected samples. Added to this is that there are currently deficiencies in the implementation of the Gavac vaccine in Cuba, which, together with a comprehensive control program that accompanied it, keeps this organism regulated at non-harmful levels. Results on the demonstrated tolerance coincided with studies by Medina et al. (2009)Medina, M.G., García, D.E., González, M.E., Cova, L.J. & Moratinos, P. 2009. Variables morfo-estructurales y de calidad de la biomasa de Tithonia diversifolia en la etapa inicial de crecimiento. Zootecnia Tropical, 27(2): 121-134, ISSN: 2542-3436. Available at: http://ve.scielo.org/pdf/zt/v27n2/art03.pdf. , who determined a low appearance value of tithonia pests and diseases under nursery conditions. These authors stated that the plant resistance is excellent, which they attribute to the insecticidal or anti-food action exerted by the secondary metabolites that make up said plant.
Conclusions
⌅The study of the entomofauna in the evaluated areas confirms the importance of the tree component in the agroecosystem, in this case the SSP with tithonia and base grass, by confirming that the system manages to maintain a biological balance of phytophagous, visitor and bioregulatory species over time, without causing economic damage to the associated plant components. Therefore, it is recommended to maintain phytosanitary surveillance in these areas by promoting increasingly diverse and resilient systems. in order to contribute to the comprehensive management of the agroecosystem.