Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-05-15T09:39:42.832Z Has data issue: false hasContentIssue false

Effect of ants on herbivory levels of Inga laurina: the interplay between space and time in an urban area

Published online by Cambridge University Press:  27 March 2023

Saulo Santos Domingos
Affiliation:
Instituto Federal de Educação, Ciência e Tecnologia Goiano, Campus Urutaí, Rod. Geraldo Silva Nascimento, km-2,5, Urutaí, GO, 75790-000, Brasil
Estevao Alves Silva*
Affiliation:
Instituto Federal de Educação, Ciência e Tecnologia Goiano, Campus Urutaí, Rod. Geraldo Silva Nascimento, km-2,5, Urutaí, GO, 75790-000, Brasil
*
Author for correspondence: Estevao Alves Silva, Email: estevao.alves@ifgoiano.edu.br

Abstract

Extrafloral nectary plants not only occur in natural areas but also in urban parks. These areas are prone to edge effects, and plants face different microenvironmental conditions. We investigated the spatial variation of ant–plant interactions in an urban park, and we examined if plants with ants would show lower herbivory levels and if it depended on habitat type (interior or edges). Seedlings of Inga laurina were set in 200-m long transects (which covered both the west and east edges, and the interior) in an urban park and then experimentally assigned to be either ant-present or ant-excluded plants. Leaf herbivory was investigated throughout the wet season and was influenced by the interaction effect between ants and habitat type. Ants decreased the herbivory on the west edge, but on the east edge results were the opposite. The east edge had higher temperature and sunlight exposure in comparison to the other sites and was assumed to disrupt the stability of ant–plant interactions. In the interior of the fragment, herbivory depended on ant presence/absence and on the location of plants along the transect. Our study highlights how the outcomes of ant–plant interactions are spatially conditioned and affected by different types of habitats.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aguilar-Peralta, JS, González-Rodríguez, A, Maldonado-López, Y, Fagundes, M, Faria, ML, Ávila-Cabadilla, LD, Álvarez-Añorve, MY and Cuevas-Reyes, P (2020) Contrasting patterns of morphology, fluctuating asymmetry and leaf herbivory in three plant species of different successional stages of a tropical dry forest. Trees 34, 10751086.CrossRefGoogle Scholar
Alves-Silva, E, Bächtold, A, Barônio, GJ, Torezan-Silingardi, HM and Del-Claro, K (2014) Ant–herbivore interactions in an extrafloral nectaried plant: are ants good plant guards against curculionid beetles? Journal of Natural History 49, 841851.CrossRefGoogle Scholar
Alves-Silva, E and Del-Claro, K (2013) Effect of post-fire resprouting on leaf fluctuating asymmetry, extrafloral nectar quality, and ant-plant-herbivore interactions. Naturwissenschaften 100, 525532.CrossRefGoogle ScholarPubMed
Alves-Silva, E and Del-Claro, K (2014) Fire triggers the activity of extrafloral nectaries, but ants fail to protect the plant against herbivores in a neotropical savanna. Arthropod-Plant Interactions 8, 233240.CrossRefGoogle Scholar
Andersen, AN (2019) Responses of ant communities to disturbance: five principles for understanding the disturbance dynamics of a globally dominant faunal group. Journal of Animal Ecology 88, 350362.CrossRefGoogle ScholarPubMed
Anjos, DV, Caserio, B, Rezende, FT, Ribeiro, SP, Del-Claro, K and Fagundes, R (2017) Extrafloral-nectaries and interspecific aggressiveness regulate day/night turnover of ant species foraging for nectar on Bionia coriacea. Austral Ecology 42, 317328.CrossRefGoogle Scholar
Aranda, R, Tibcherani, M, Nacagava, VAF, de Carvalho, SS and de Souza, PR (2022) The role of urban savannah fragments and their characteristics for the conservation of ants (Hymenoptera: Formicidae) in central Brazil. Community Ecology 23, 115127.CrossRefGoogle Scholar
Aristizábal, N and Metzger, JP (2019) Landscape structure regulates pest control provided by ants in sun coffee farms. Journal of Applied Ecology 56, 2130.CrossRefGoogle Scholar
Bächtold, A, Silva, EA and Del-Claro, K (2016) Ants, plant characteristics and habitat conservation status affect the occurrence of myrmecophilous butterflies on an extrafloral nectaried Malpighiaceae. Studies on Neotropical Fauna and Environment 51, 112120.Google Scholar
Bixenmann, RJ, Coley, PD and Kursar, TA (2013) Developmental changes in direct and indirect defenses in the young leaves of the Neotropical tree genus Inga (Fabaceae). Biotropica 45, 175184.CrossRefGoogle Scholar
Bolger, DT, Suarez, AV, Crooks, KR, Morrison, SA and Case, TJ (2000) Arthropods in urban habitat fragments in Southern California: area, age, and edge effects. Ecological Applications 10, 12301248.CrossRefGoogle Scholar
Burger, HF, Vondráčková, K, Skłodowski, M, Koid, Q, Dent, DH, Wallace, K and Fayle, TM (2021) Protection from herbivores varies among ant genera for the myrmecophilic plant Leea aculeata in Malaysian Borneo. Asian Myrmecology 14, 116.Google Scholar
Calixto, ES, Novaes, LR, Santos, DFB, Lange, D, Moreira, X and Del-Claro, K (2021) Climate seasonality drives ant-plant-herbivore interactions via plant phenology in an extrafloral nectary-bearing plant community. Journal of Ecology 109, 639651.CrossRefGoogle Scholar
Câmara, T, Almeida, WR, Tabarelli, M, Andersen, AN and Leal, IR (2017) Habitat fragmentation, EFN-bearing trees and ant communities: ecological cascades in Atlantic Forest of northeastern Brazil. Austral Ecology 42, 3139.CrossRefGoogle Scholar
Câmara, T, Leal, IR, Blüthgen, N, Oliveira, FMP, Queiroz, RTD and Arnan, X (2018) Effects of chronic anthropogenic disturbance and rainfall on the specialization of ant–plant mutualistic networks in the Caatinga, a Brazilian dry forest. Journal of Animal Ecology 87, 10221033.CrossRefGoogle ScholarPubMed
Cantone, S (2018) Winged Ants in the city of São Paulo, Brazil: analysis of the mating flight: 47–54.Google Scholar
Christianini, AV and Oliveira, PS (2012) Edge effects decrease ant-derived benefits to seedlings in a neotropical savanna. Arthropod-Plant Interactions 7, 191199.CrossRefGoogle Scholar
Clarke, KM, Fisher, BL and Lebuhn, G (2008) The influence of urban park characteristics on ant (Hymenoptera, Formicidae) communities. Urban Ecosystems 11, 317334.CrossRefGoogle Scholar
Coley, PD (1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74, 531536.CrossRefGoogle ScholarPubMed
Coley, PD, Lokvam, J, Rudolph, K, Bromberg, K, Sackett, TE, Wright, L, Brenes-Arguedas, T, Dvorett, D, Ring, S, Clark, A, Baptiste, C, Pennington, RT and Kursar, TA (2005) Divergent defensive strategies of young leaves in two species of Inga . Ecology 86, 26332643.CrossRefGoogle Scholar
Cruz Rocha, ML, Cristaldo, PF, Santos Lima, PS, Dos Santos, AT, Do Sacramento, JJM, Santana, DL, Dos Santos Oliveira, BV, Bacci, L and Albano Araújo, AP (2019) Production of extrafloral nectar in the Neotropical shrub Turnera subulata mediated by biotic and abiotic factors. Flora: Morphology, Distribution, Functional Ecology of Plants 260, 151483.CrossRefGoogle Scholar
Del-Claro, K and Marquis, RJ (2015) Ant species identity has a greater effect than fire on the outcome of an ant protection system in Brazilian Cerrado. Biotropica 47, 459467.CrossRefGoogle Scholar
Del-Claro, K, Rico-Gray, V, Torezan-Silingardi, HM, Alves-Silva, E, Fagundes, R, Lange, D, Dáttilo, W, Vilela, AA, Aguirre, A and Rodriguez-Morales, D (2016) Loss and gains in ant–plant interactions mediated by extrafloral nectar: fidelity, cheats, and lies. Insectes Sociaux 63, 207221.CrossRefGoogle Scholar
Dudt, JF and Shure, DJ (1994) The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75, 8698.CrossRefGoogle Scholar
Fagundes, R, Dáttilo, W, Ribeiro, SP, Rico-Gray, V, Jordano, P and Del-Claro, K (2017) Differences among ant species in plant protection are related to production of extrafloral nectar and degree of leaf herbivory. Biological Journal of the Linnean Society 122, 7183.CrossRefGoogle Scholar
Franco, MS and Cogni, R (2013) Common-garden experiments reveal geographical variation in the interaction among Crotalaria pallida (Leguminosae: Papilionideae), Utetheisa ornatrix L. (Lepidoptera: Arctiidae), and extrafloral nectary visiting ants. Neotropical Entomology 42, 223229.CrossRefGoogle ScholarPubMed
Fuente, MAS and Marquis, RJ (1999) The role of ant-tended extrafloral nectaries in the protection and benefit of a Neotropical rainforest tree. Oecologia 118, 192202.CrossRefGoogle ScholarPubMed
García-Jain, SE, Maldonado-López, Y, Oyama, K, Fagundes, M, de Faria, ML, Espírito-Santo, MM and Cuevas-Reyes, P (2021) Effects of forest fragmentation on plant quality, leaf morphology and herbivory of Quercus deserticola: is fluctuating asymmetry a good indicator of environmental stress? Trees 2021, 115. Springer.Google Scholar
González-Teuber, M, Silva Bueno, JC, Heil, M and Boland, W (2012) Increased host investment in extrafloral nectar (EFN) improves the efficiency of a mutualistic defensive service. PLoS ONE 7, e46598.CrossRefGoogle ScholarPubMed
Jones, IM and Koptur, S (2015) Quantity over quality: light intensity, but not red/far-red ratio, affects extrafloral nectar production in Senna mexicana var. chapmanii . Ecology and Evolution 5, 41084114.CrossRefGoogle Scholar
Katayama, N and Suzuki, N (2011) Anti-herbivory defense of two Vicia species with and without extrafloral nectaries. Plant Ecology 212, 743752.CrossRefGoogle Scholar
Kelly, CA (1986) Extrafloral nectaries: ants, herbivores and fecundity in Cassia fasciculata . Oecologia 69, 600605.CrossRefGoogle ScholarPubMed
Kersch, MF and Fonseca, CR (2005) Abiotic factors and the conditional outcome of an ant-plant mutualism. Ecology 86, 21172126.CrossRefGoogle Scholar
Koptur, S (1984) Experimental evidence for defense of Inga (Mimosoideae) saplings by ants. Ecology 65, 17871793.CrossRefGoogle Scholar
Koptur, S (1985) Alternative defenses against herbivores in Inga (Fabaceae: Mimosoideae) over an elevational gradient. Ecology 66, 16391650.CrossRefGoogle Scholar
Kost, C and Heil, M (2005) Increased availability of extrafloral nectar reduces herbivory in Lima bean plants (Phaseolus lunatus, Fabaceae). Basic and Applied Ecology 6, 237248.CrossRefGoogle Scholar
Kunert, N, Aparecido, LMT, Higuchi, N, Santos, JDos and Trumbore, S (2015) Higher tree transpiration due to road-associated edge effects in a tropical moist lowland forest. Agricultural and Forest Meteorology 213, 183192.CrossRefGoogle Scholar
Kursar, TA, Dexter, KG, Lokvam, J, Pennington, RT, Richardson, JE, Weber, MG, Murakami, ET, Drake, C, Mcgregor, R and Coley, PD (2009) The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga . Proceedings of the National Academy of Sciences of the United States of America 106, 1807318078.CrossRefGoogle ScholarPubMed
Lange, D, Dáttilo, W and Del-Claro, K (2013) Influence of extrafloral nectary phenology on ant-plant mutualistic networks in a neotropical savanna. Ecological Entomology 38, 463469.CrossRefGoogle Scholar
Leal, LC, Andersen, AN and Leal, IR (2015) Disturbance winners or losers? Plants bearing extrafloral nectaries in Brazilian Caatinga. Biotropica 47, 468474.CrossRefGoogle Scholar
McFrederick, QS and LeBuhn, G (2006) Are urban parks refuges for bumble bees Bombus spp. (Hymenoptera: Apidae)? Biological Conservation 129, 372382.CrossRefGoogle Scholar
Melo, TS, Koch, EBA, Andrade, ARS, Travassos, MLO, Peres, MCL and Delabie, JHC (2022) Ants (Hymenoptera: Formicidae) in different green areas in the metropolitan region of Salvador, Bahia state, Brazil. Brazilian Journal of Biology 82, 16.CrossRefGoogle Scholar
Mendonça, AH, Russo, C, Melo, ACG and Durigan, G (2015) Edge effects in savanna fragments: a case study in the cerrado. Plant Ecology and Diversity 8, 493503.CrossRefGoogle Scholar
Menke, SB, Guénard, B, Sexton, JO, Weiser, MD, Dunn, RR and Silverman, J (2011) Urban areas may serve as habitat and corridors for dry-adapted, heat tolerant species; an example from ants. Urban Ecosystems 14, 135163.CrossRefGoogle Scholar
Millán-Cañongo, C, Orona-Tamayo, D and Heil, M (2014) Phloem sugar flux and jasmonic acid-responsive cell wall invertase control extrafloral nectar secretion in Ricinus communis . Journal of Chemical Ecology 40, 760769.CrossRefGoogle ScholarPubMed
Mody, K and Linsenmair, KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecological Entomology 29, 217225.CrossRefGoogle Scholar
Monique, K, De Souza, GR, Calixto, ES and Silva, EA (2022) Temporal variation in the effect of ants on the fitness of myrmecophilic plants: seasonal effect surpasses periodic benefits. Science of Nature 109, 19.CrossRefGoogle ScholarPubMed
Munhae, C de B, Souza-Campana, DR de, Kamura, CM and Castro Morini, MS de (2015) Ant communities (Hymenoptera: Formicidae) in urban centers of the Alto Tietê, São Paulo, Brazil. Arquivos do Instituto Biológico 82, 15.CrossRefGoogle Scholar
Munhae, CB, Bueno, ZAFN, Morini, MSC and Silva, RR (2009) Composition of the ant fauna (Hymenoptera: Formicidae) in public squares in Southern Brazil. Sociobiology 53, 455472.Google Scholar
Nascimento, EA and Del-Claro, K (2010) Ant visitation to extrafloral nectaries decreases herbivory and increases fruit set in Chamaecrista debilis (Fabaceae) in a Neotropical savanna. Flora 205, 754756.CrossRefGoogle Scholar
Newman, JR and Wagner, D (2013) The influence of water availability and defoliation on extrafloral nectar secretion in quaking aspen (Populus tremuloides). Botany 91, 761767.CrossRefGoogle Scholar
Nielsen, AB, van den Bosch, M, Maruthaveeran, S and van den Bosch, CK (2014) Species richness in urban parks and its drivers: a review of empirical evidence. Urban Ecosystems 17, 305327.CrossRefGoogle Scholar
Nikiforou, C and Manetas, Y (2017) Ecological stress memory: evidence in two out of seven species through the examination of the relationship between leaf fluctuating asymmetry and photosynthesis. Ecological Indicators 74, 530534.CrossRefGoogle Scholar
Nogueira, A, Baccaro, FB, Leal, LC, Rey, PJ, Lohmann, LG and Bronstein, JL (2020) Variation in the production of plant tissues bearing extrafloral nectaries explains temporal patterns of ant attendance in Amazonian understorey plants. Journal of Ecology 108, 15781591.CrossRefGoogle Scholar
Nogueira, A, Guimarães, E, Machado, S and Lohmann, L (2012) Do extrafloral nectaries present a defensive role against herbivores in two species of the family Bignoniaceae in a Neotropical savannas? Plant Ecology 213, 289301.CrossRefGoogle Scholar
Nogueira, A, Rey, PJ, Alcántara, JM, Feitosa, RM and Lohmann, LG (2015) Geographic mosaic of plant evolution: extrafloral nectary variation mediated by ant and herbivore assemblages. PLoS ONE 10, 124.CrossRefGoogle ScholarPubMed
Pacheco, R and Vasconcelos, HL (2007) Invertebrate conservation in urban areas: ants in the Brazilian Cerrado. Landscape and Urban Planning 81, 193199.CrossRefGoogle Scholar
Palmer, TM and Brody, AK (2007) Mutualism as reciprocal exploitation: African plant-ants defend foliar but not reproductive structures. Ecology 88, 30043011.CrossRefGoogle Scholar
Pereira, CC, Boaventura, MG, de Castro, GC and Cornelissen, T (2020) Are extrafloral nectaries efficient against herbivores? Herbivory and plant defenses in contrasting tropical species. Journal of Plant Ecology 13, 423430.CrossRefGoogle Scholar
Pereyra, M, Pol, RG and Galetto, L (2015) Does edge effect and patch size affect the interaction between ants and Croton lachnostachyus in fragmented landscapes of Chaco forest? Arthropod-Plant Interactions 9, 175186.CrossRefGoogle Scholar
Polli, A, Romagnolo, MB, Souza, LA de and Pastorini, LH (2020) Influence of the functional traits of seeds on germination dynamics and morphofunctional pattern of the seedlings. Acta Scientiarum. Biological Sciences 42, e52154.CrossRefGoogle Scholar
Raupp, PP, Gonçalves, RV, Calixto, ES and Anjos, DV (2020) Contrasting effects of herbivore damage type on extrafloral nectar production and ant attendance. Acta Oecologica 108, 17.CrossRefGoogle Scholar
Ribeiro, FM, Sibinel, N, Ciocheti, G and Campos, AEC (2012) Analysis of ant communities comparing two methods for sampling ants in an urban park in the city of São Paulo, Brazil. Sociobiology 59, 971984.Google Scholar
Rosumek, F, Silveira, F, de S Neves, F., de U Barbosa, N, Diniz, L, Oki, Y, Pezzini, F, Fernandes, G and Cornelissen, T (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160, 537549.CrossRefGoogle ScholarPubMed
Santos, JC, Alves-Silva, E, Cornelissen, TG and Fernandes, GW (2013) The effect of fluctuating asymmetry and leaf nutrients on gall abundance and survivorship. Basic and Applied Ecology 14, 489495.CrossRefGoogle Scholar
Santos, MN, Delabie, JHC and Queiroz, JM (2019) Biodiversity conservation in urban parks: a study of ground-dwelling ants (Hymenoptera: Formicidae) in Rio de Janeiro City. Urban Ecosystems 22, 927942.CrossRefGoogle Scholar
Silva, CHF, Arnan, X, Andersen, AN and Leal, IR (2019) Extrafloral nectar as a driver of ant community spatial structure along disturbance and rainfall gradients in Brazilian dry forest. Journal of Tropical Ecology 35, 280287.CrossRefGoogle Scholar
Silva, EA, Anjos, D, Bächtold, A, Lange, D, Maruyama, PK, Del-Claro, K and Mody, K (2020) To what extent is clearcutting vegetation detrimental to the interactions between ants and Bignoniaceae in a Brazilian savanna? Journal of Insect Conservation 24, 103114.CrossRefGoogle Scholar
Souza-Campana, DR, Carvalho, ACN, Canali, M, Silva, OGM, Morini, MSC and Fujihara, RT (2020) A rapid survey of ground-dwelling ants (Hymenoptera: Formicidae) in an urban park from state of São Paulo, Brazil. Brazilian Journal of Biology 80, 682684.CrossRefGoogle Scholar
Thompson, JN (2005) The geographic mosaic of coevolution. Chicago: University of Chicago Press, 442 p.CrossRefGoogle Scholar
Uriarte, M, Canham, CD, Thompson, J and Zimmerman, JK (2004) A neighborhood analysis of tree growth and survival in a hurricane-driven tropical forest. Ecological Monographs 74, 591614.CrossRefGoogle Scholar
Wang, H, Lei, J, Li, S, Fan, J, Li, Y, Sun, S and Chang, Q (2009) Effect of the shelterbelt along the Tarim Desert Highway on air temperature and humidity. Chinese Science Bulletin 53, 4152.Google Scholar
Wirth, R, Meyer, ST, Leal, IR and Tabarelli, M (2008) Plant herbivore interactions at the forest edge. Progress in Botany 69, 423448.CrossRefGoogle Scholar
Yamawo, A, Tagawa, J, Hada, Y and Suzuki, N (2014) Different combinations of multiple defence traits in an extrafloral nectary-bearing plant growing under various habitat conditions. Journal of Ecology 102, 238247.CrossRefGoogle Scholar
Supplementary material: File

Domingos and Alves Silva supplementary material

Domingos and Alves Silva supplementary material 1

Download Domingos and Alves Silva supplementary material(File)
File 808.5 KB
Supplementary material: File

Domingos and Alves Silva supplementary material

Domingos and Alves Silva supplementary material 2

Download Domingos and Alves Silva supplementary material(File)
File 477.1 KB