Effect of patch size of the exotic host plant Calotropis procera (Apocynaceae) on herbivory

Abstract

Calotropis procera is a xerophytic perennial milkweed shrub native to Asia and Africa, which currently is also widely distributed throughout the Brazilian Caatinga. C. procera is well defended against herbivores, especially with latex and toxic steroidal cardenolides. The goal of this study was to evaluate how patch size of this exotic host plant affect insect herbivory. Eight patches were selected containing a varied number of C. procera individuals (5, 8, 29, 31, 55, 79, 116, and 172 individuals/patch) in the Caatinga. Patches were divided into four categories according to the number of C. procera individuals: very small (5 and 8), small (29 and 31), intermediate (55 and 79), and large (116 and 172). The percentage of herbivory was greater in patch categories with more individuals. Among the herbivorous insects associated with C. procera, larvae of Danaus spp. (Lepidoptera: Nymphalidae) were commonly observed feeding on all patches. These herbivores present specialized behaviors to circumvent the presence of latex on the host leaves. Adult Danaus spp. females probably had higher probability to find large patches of C. procera, leaving a greater abundance of eggs and, consequently, increasing the herbivory by their larvae in these patches. In contrast to immigration tendency, emigration from large patches may be lower, because there is a higher probability of finding resources (e. g. suitable C. procera leaves) inside large patches compared with small patches. We conclude that patch size of the host plant C. procera is a major factor affecting herbivory.

Keywords:
Caatinga; Danaus; Insect-plant interactions; Invasive species; Resource concentration hypothesis

The distribution of insect herbivores is primarily limited by the occurrence of their host plants. At a local scale, individual plants can vary in architectural complexity and herbivorous insects are more likely to be found on the most vigorous plants within a plant population and/or on the most vigorous modules within a plant (Price, 1991; Faria and Fernandes, 2001; Cornelissen et al., 2008). At the landscape scale, plant density (the number of individuals of a given species that occurs within a given sample unit or study area) and patch size (the number of host plants or the geographical extent of the stand) are important factors that can affect the abundance and diversity of insect herbivores (Root, 1973; Raupp and Denno, 1979; Kéry et al., 2001; Cassel-Lundhagen et al., 2008).

The resource concentration hypothesis (Root, 1973) states that larger host plant patches should have large insect densities because the probability of insects, particularly specialists, finding a large path is higher and the probability of an insect leaving a large patch is lower. However, several studies addressing the effects of host plant patch size on herbivore abundance have shown variable effects (e.g., Bach, 1988; Kareiva, 1983; Bukovinszky et al., 2010). Part of the inconsistency of the results in patch size experiments can be attributed to species-specific differences in the dispersal abilities of herbivorous insects and to the wide variety of systems studied. For example, the largest patches between studies ranged from a few square meters to dozens of hectares (e.g. Bach, 1988; Raupp and Denno, 1979; McCauley, 1991; Bukovinszky et al., 2010).

Calotropis procera (Aiton) WT Aiton (Apocynaceae) is a xerophytic perennial milkweed shrub native to Asia and Africa, which has been widely introduced as an ornamental plant into many other parts of the world (Hassan et al., 2015; Fig. 1A). In Brazil, its tolerance to drought and to acidic and nutrient-poor soils allowed the expansion into the Cerrado and Caatinga biome domains (Ulhôa et al., 2007; Rangel and Nascimento, 2011). In addition, this invasive exotic species presents rapid growth, dispersion by wind and easy propagation, which have allowed the formation of large populations mainly in disturbed areas, such as in pastures and roadsides (Ulhôa et al., 2007; Fabricante et al., 2013). The presence of patches of C. procera with vigorous and green leaves throughout the year may represent an important resource for herbivorous insects, especially in strongly seasonal environments such as the Brazilian Caatinga. Despite the fact that this species is very well defended against herbivores, especially with latex and toxic steroidal cardenolides (Malcolm, 1991; Agrawal et al., 2012), many insects from Coleoptera, Hemiptera and Lepidoptera orders have been reported consuming C. procera leaves (Chandra et al., 2011; Al Dhafer et al., 2011).

Figure 1
(A) Adult individual of Calotropis procera in a pasture area in the Caatinga, Pernambuco, Brazil; (B) early and (C) late instars of Danaus erippus.

The objective of this study was to evaluate how patch size of the exotic host plant C. procera affects leaf herbivory. We tested the resource concentration hypothesis (Root, 1973), and predicted that there will be a greater percentage of leaf herbivory on patches with more individuals of the host plant C. procera.

The study was carried out between March and April 2006 in an area belonging to the Agronomic Institute of Pernambuco, located in the municipality of Serra Talhada, Pernambuco, Brazil. The climate of the region is seasonal with an average annual precipitation of approximately 800 mm, concentrated from January to May, and annual average temperature of 26˚C (Sampaio, 1995). The local biome is Caatinga, dominated by an arboreal-shrubby physiognomy (Ferraz et al., 1998). The herbaceous stratum is not very dense and is mainly composed of annual plants that grow only in the rainy season (Sampaio, 1995).

To evaluate the effect of patch size (number of individuals) on insect herbivory eight patches were selected containing a varied number of C. procera individuals (5, 8, 29, 31, 55, 79, 116 and 172 individuals / patch). In each patch all individuals were marked and had their heights estimated (co-variable). To estimate the percentage leaf herbivory in the patches, all plants higher than one meter and with more than ten branches were pre-selected. Of these, five were randomly selected in each patch. From each individual, three to six young stems were randomly selected, from which their leaves were collected, for a total of approximately 200 leaves per patch. Each C. procera individual was surveyed once. The leaf area removed was calculated by dividing the sum of all areas removed from a leaf by the total area of the respective leaf. The leaf images were analyzed using the Image Tool 1.1 program. The percentage of herbivory on each plant individual was determined by averaging the leaf area removed from each stem per individual.

First, a correlation analysis was performed between the independent variables (patch size and average patch height). The variables showed a strong correlation with each other (r = 0.716, p < 0.001), and therefore, average patch height was discarded from the model (see Clarke and Warwick, 2001). Patches were divided into four categories according to the number of C. procera individuals: very small (5 and 8), small (29 and 31), intermediate (55 and 79), and large (116 and 172). A Generalized Linear Model with a “Quasi-binomial” distribution of errors was used to test whether the percentage of herbivory would be higher in patch categories (very small, small, intermediate, and large) with a greater number of individuals. Analysis of variance (ANOVA) was used to test for differences in leaf herbivory between these categories. The package “lsmeans” was used for a posteriori comparisons (Lenth, 2017). The statistical analyses were conducted with the R software (R Core Team, 2020).

The percentage of branches with at least one leaf damaged was high in all patches (88-100%), while the percentage of herbivory varied from 2.78% to 11.74% among patches. The percentage of herbivory was greater in patch categories with more individuals (deviance = 0.974; F = 10.442; p < 0.0001; Fig. 2). Despite no quantitative data on the abundance of the insect herbivore species associated with C. procera in this study, larvae of Danaus spp. (Lepidoptera: Nymphalidae) were commonly observed feeding on all patches (M.F.V. Rodrigues-Menelau personal communication). Larvae of the three Danaus species that occur in the Brazilian Caatinga, D. erippus, D. gilippus and D. eresimus, were observed feeding on C. procera. In contrast, chewing insects from other orders, such as Coleoptera and Orthoptera, were observed feeding in few individuals of C. procera (n < 10; M.F.V. Rodrigues-Menelau personal communication).

Figure 2
Boxplots of the percentage of herbivory between patches of C. procera of different sizes (number of individuals) in the Caatinga, Pernambuco, Brazil. Each circle represents the average percentage of herbivory of the branches of each individual sampled. The horizontal thick grey band represents the median value, the boxplot margins indicate first and third quartiles, the whiskers represent the maximum/minimum value within one and a half times the interquartile range.

The resource concentration hypothesis was supported in our study system, since we confirm our prediction that Calotropis procera plants within patches with a greater number of individuals would be more attacked by herbivorous insects than those within patches with few host plants. Previous studies have reported Danaus spp. as important herbivores feeding on milkweed species, presenting specialized behaviors to circumvent the presence of latex (Rodrigues et al., 2010; Ferreira and Rodrigues, 2015). Early instars of Danaus spp. have been observed performing both trenching and vein-cutting on milkweeds, while late instars, which have already acquired greater resistance to latex, are able to feed directly on the leaf margins (Rodrigues et al., 2010; Ferreira and Rodrigues, 2015; Fig. 1B and Fig. 1C). In addition, compared with the small number of South American herbaceous milkweed species (genus Asclepias), C. procera is a woody milkweed that is probably very apparent and extremely easy to find by specialized Danaus spp.

Positive relationships between host population size and the occurrence of associated specialized species have been reported for other lepidopterans (e.g., Förare and Solbreck, 1997; Kéry et al., 2001; Cassel-Lundhagen et al., 2008; but see Grez and Gonzalez, 1995). For example, population size of the butterfly Cupido minimus was positively related to the coverage of its larval food plant Anthyllis vulneraria (Krauss et al., 2004). Similarly, populations of the butterfly Maculinea rebeli were both more likely and larger on larger populations of its host plant Gentiana cruciata (Kéry et al., 2001).

Previous studies showed that specialized butterflies should have a higher probability of immigrating to large patches, which are a larger target (Kéry et al., 2001; Krauss et al., 2003). In our study, adult Danaus spp. females probably had higher probability to find large patches of C. procera, leaving a greater abundance of eggs and, consequently, increasing the herbivory by their larvae in these patches. In contrast to immigration tendency, emigration from large patches may be lower, because there is a higher probability of finding resources (e. g. suitable C. procera leaves) inside large patches compared with small patches (Root, 1973). Thomas and Jones (1993) demonstrated that the probability of colonization by the butterfly Hesperia comma increased with increase of the patch area of its host plant, while probability of local extinction declined with increasing patch area. Similarly, a study showed that the extinction rates of specialized butterfly species decreased with increasing fragment size (Krauss et al., 2003).

We conclude that patch size of the host plant C. procera is a major factor affecting herbivory. Despite no quantitative data on the abundance of the insect herbivores associated with C. procera, we highlight the presence of Danaus species commonly feeding on this exotic host plant. Much is yet to be learned on the colonization of C. procera by these Danaus species in the Brazilian Caatinga, and this might represents an interesting system in which one can test many important long standing hypotheses on insect plant relationships as well as to investigate how population dynamics of the different Danaus species may differ from each other.

Acknowledgments

We thank PROCAD/CAPES (grant number 0166057) for financing the project. This study was part of MFV Rodrigues-Menelau ’MSc at UFPE that was supported by CNPq. We also thank UFRPE and IPA of Serra Talhada for logistical support. SN thanks CAPES for the postdoctoral researcher scholarship (CNPq-CAPES-PELD - 88887.142635/2017–00). GWF and JSA thank CNPq for the productivity grant.

References

• Agrawal, A. A., Petschenka, G., Bingham, R. A., Weber, M. G., Rasmann, S., 2012. Toxic cardenolides: chemical ecology and coevolution of specialized plant–herbivore interactions. New Phytol. 194, 28-45.
• Al Dhafer, H. M., Aldryhim, Y. N., Elgharbawy, A. A., Fadl, H. H., 2011. Insects associated with milkweed Calotropis procera (Ait.) Ait. in the Ibex reserve in the central region of the Kingdom of Saudi Arabia. Entomol. News 122, 233-246.
• Bach, C. E., 1988. Effects of host plant patch size on herbivore density: patterns. Ecology 69, 1090-1102.
• Bukovinszky, T., Gols, R., Kamp, A., de Oliveira-Domingues, F., Hambäck, P. A., Jongema, Y., Bezemer, T. M., Dicke, M., van Dam, N. M., Harvey, J. A., 2010. Combined effects of patch size and plant nutritional quality on local densities of insect herbivores. Basic Appl. Ecol. 11, 396-405.
• Cassel-Lundhagen, A., Sjögren-Gulve, P., Berglind, S. Å., 2008. Effects of patch characteristics and isolation on relative abundance of the scarce heath butterfly Coenonympha hero (Nymphalidae). J. Insect Conserv. 12, 477-482.
• Chandra, K., Kushwaha, S., Gupta, D., Singh, S. P., 2011. Record of some insects associated with Calotropis procera (Asclepiadaceae) in Jabalpur District (MP), India. Natl. J. Sci. 8, 77-87.
• Clarke, K. R., Warwick, R. M., 2001. Change in marine communities: an approach to statistical analyses and interpretation. PRIMER-E Ltd, Plymouth.
• Cornelissen, T., Fernandes, G. W., Vasconcellos‐Neto, J., 2008. Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis. Oikos 117, 1121-1130.
• Fabricante, J. R., Oliveira, M. N. A., Siqueira Filho, J. A., 2013. Aspectos da ecologia de Calotropis procera (Apocynaceae) em uma área de Caatinga alterada pelas obras do Projeto de Integração do Rio São Francisco em Mauriti, CE. Rodriguésia 64, 647-654.
• Faria, M. L., Fernandes, G. W., 2001. Vigour of a dioecious shrub and attack by galling herbivore. Ecol. Entomol. 26, 37-45.
• Ferraz, E. M. N., Rodal, M. J. N., Sampaio, E. V., Pereira, R. D. C. A., 1998. Composição florística em trechos de vegetação de caatinga e brejo de altitude na região do Vale do Pajeú, Pernambuco. Braz. J. Bot. 21, 7-15.
• Ferreira, P. P., Rodrigues, D., 2015. Sabotaging behavior and decision-making in larvae of the queen butterfly Danaus gilippus. J. Insect Behav. 28, 460-472.
• Förare, J., Solbreck, C., 1997. Population structure of a monophagous moth in a patchy landscape. Ecol. Entomol. 22, 256-263.
• Grez, A. A., Gonzalez, R. H., 1995. Resource concentration hypothesis: effect of host plant patch size on density of herbivorous insects. Oecologia 103, 471-474.
• Hassan, L. M., Galal, T. M., Farahat, E. A., El-Midany, M. M., 2015. The biology of Calotropis procera (Aiton) WT. Trees (Berl.) 29, 311-320.
• Kareiva, P., 1983. Influence of vegetation texture on herbivore populations: resource concentration and herbivore movement. In: Denno, R.F., McClure, M.S. (Eds.), Variable Plants and Herbivores in Natural and Managed Systems. Academic Press, New York, pp. 259-289.
• Kéry, M., Matthies, D., Fischer, M., 2001. The effect of plant population size on the interactions between the rare plant Gentiana cruciata and its specialized herbivore Maculinea rebeli. J. Ecol. 89, 418-427.
• Krauss, J., Steffan-Dewenter, I., Tscharntke, T., 2003. Local species immigration, extinction, and turnover of butterflies in relation to habitat area and habitat isolation. Oecologia 137, 591-602.
• Krauss, J., Steffan-Dewenter, I., Tscharntke, T., 2004. Landscape occupancy and local population size depends on host plant distribution in the butterfly Cupido minimus. Biol. Conserv. 120, 355-361.
• Lenth, R. V., 2017. Using lsmeans. Available in: https://cran.r-project.org/web/packages/lsmeans/vignettes/using-lsmeans.pdf (accessed 13 March 2020).
  » https://cran.r-project.org/web/packages/lsmeans/vignettes/using-lsmeans.pdf
• Malcolm, S. B. 1991. Cardenolide-mediated interactions between plants and herbivores. In: Rosenthal G.A., Berenbaum, M.R. (Eds.), Herbivores: Their Interaction with Secondary Plant Metabolites: The Chemical Participants. Academic Press, San Diego, pp. 251-296.
• McCauley, D. E., 1991. The effect of host plant patch size variation on the population structure of a specialist herbivore insect, Tetraopes tetraophthalmus. Evolution 45, 1675-1684.
• Price, P. W., 1991. The plant vigour hypothesis and herbivore attack. Oikos 62, 244-251.
• R Core Team, 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
• Rangel, E. D. S., Nascimento, M. T., 2011. Ocorrência de Calotropis procera (Ait.) R. Br. (Apocynaceae) como espécie invasora de restinga. Acta Bot. Bras. 25, 657-663.
• Raupp, M. J., Denno, R. F., 1979. The influence of patch size on a guild of sap-feeding insects that inhabit the salt marsh grass Spartina patens. Environ. Entomol. 8, 412-417.
• Rodrigues, D., Maia, P. H., Trigo, J. R., 2010. Sabotaging behaviour and minimal latex of Asclepias curassavica incur no cost for larvae of the southern monarch butterfly Danaus erippus. Ecol. Entomol. 35, 504-513.
• Root, R. B., 1973. Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol. Monogr. 43, 95-124.
• Sampaio, E. V. S. B. 1995. Overview of the Brazilian Caatinga. In: Bullock, S.H., Mooney, H.A., Medina E. (Eds.), Seasonally Dry Tropical Forests. Cambridge University Press, Cambridge, pp. 35-63.
• Thomas, C. D., Jones, T. M., 1993. Partial recovery of a skipper butterfly (Hesperia comma) from population refuges: lessons for conservation in a fragmented landscape. J. Anim. Ecol. 62, 472-481.
• Ulhôa, N., Almeida-Cortez, J. S., Fernandes, G. W., 2007. Uma estranha na paisagem. Cienc. Hoje 41, 70-73.

Edited by

Associate Editor: Lucas Kaminski

Publication Dates

• Publication in this collection
  24 Aug 2020
• Date of issue
  2020

History

• Received
  13 Mar 2020
• Accepted
  27 June 2020