Leaf changes in Avicennia schaueriana following a massive herbivory event by Hyblaea puera (Lepidoptera) in South Brazil Mudanças foliares em ...
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Brazilian Journal of Development 47275
ISSN: 2525-8761
Leaf changes in Avicennia schaueriana following a massive herbivory
event by Hyblaea puera (Lepidoptera) in South Brazil
Mudanças foliares em Avicennia schaueriana após um grande evento
de herbivoria por Hyblaea puera (Lepidoptera) no Sul do Brasil
DOI:10.34117/bjdv7n5-233
Recebimento dos originais: 07/04/2021
Aceitação para publicação: 12/05/2021
Amanda Martins Ruthes
Laboratory of Plant Morphology and Ecology, Post-graduate Program in Health and
Environmental, University of Joinville Region, R. Paulo Maschitzki 10, 89219-710,
Joinville, SC, Brazil
Maiara Matilde da Silva
Post-graduate Program in Ecology and Conservation, Federak University of Paraná,
Box 19031, 81531-990 Curitiba, PR, Brazil
João Carlos Ferreira de Melo Júnior
Laboratory of Plant Morphology and Ecology, Post-graduate Program in Health and
Environmental, University of Joinville Region, R. Paulo Maschitzki 10, 89219-710,
Joinville, SC, Brazil
E-mail: joao.melo@univille.br
ABSTRACT
(Leaf changes in Avicennia schaueriana following a massive herbivory event by Hyblaea
puera (Lepidoptera) in South Brazil) Herbivory is an interaction that can change the
structure of plant communities in two main ways: by causing death and reducing plant
populations; and by changing leaf characteristics of plants that, secondarily, changes
interactions of plants with the biotic and abiotic environment. Leaf defense and nutritional
attributes of Avicennia schaueriana were comparatively evaluated after a massive
herbivory event by the exotic species Hyblaea puera (Lepidoptera: Hyblaeidae) in the
mangrove of Babitonga Bay, Joinville, SC, Brazil. The leaf attributes differed between
the A. schaueriana control group and group that suffered a massive herbivory attack. The
specific leaf area (SLA) was smaller in the group that suffered the injury from herbivory
and, thus, the leaves were harder. In addition, there was a reduction in water content that
made the leaves less nutritious. Secondary compounds were present in more mesophyll
tissues in the plants that suffered herbivory compared to the control group. These results
suggest that the plants respond to herbivory through changes in the leaves that reduce the
preference of the insects.
Keywords: plant herbivory, tropical mangrove, environmental quality
RESUMO
A herbivoria é uma interação que pode mudar a estrutura das comunidades de plantas de
duas maneiras principais: causando a morte e reduzindo as sua populações; ou alterando
as características das folhas das plantas que, secundariamente, alteram as interações das
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plantas com o ambiente biótico e abiótico. A defesa foliar e os atributos nutricionais de
Avicennia schaueriana foram avaliados comparativamente após um evento de herbivoria
massiva pela espécie exótica Hyblaea puera (Lepidoptera: Hyblaeidae) no manguezal da
baía Babitonga, Joinville, SC, Brasil. Os atributos foliares diferiram entre o grupo
controle de A. schaueriana e o grupo que sofreu um ataque massivo de herbivoria. A área
foliar específica (SLA) foi menor no grupo que sofreu o dano por herbivoria e, portanto,
as folhas ficaram mais duras. Além disso, houve redução do teor de água que tornou as
folhas menos nutritivas. Compostos secundários estiveram presentes em mais tecidos do
mesofilo nas plantas que sofreram herbivoria em comparação ao grupo controle. Esses
resultados sugerem que as plantas respondem à herbivoria por meio de mudanças nas
folhas que reduzem a preferência dos insetos.
Palavras-chave: herbivoria vegetal, manguezal tropical, qualidade ambiental
1 INTRODUCTION
Herbivory is one of the most common interactions in natural environments due to
the high diversity of extant plants and insects. Rates of herbivory are controlled by leaf
characteristics, such as presence of epidermal appendages (Abdala-Roberts & Parra-
Tabla 2005), presence of a thick cuticle of varying chemical composition (Eigenbrode &
Espelie 1995), amount of calcium oxalate crystals (Franceschi & Nakata 2005), and
chemical compounds in cells that repel or are toxic to insects (Kursar & Coley 2003).
Plants that occupy shaded habitats on soils with high water availability and high
concentrations of nutrients develop more nutritious palatable leaves and, consequently,
are damaged more by herbivores (Muth et al. 2008; LoPresti 2017). On the other hand,
plants that occur in environments with scarce resources or conditions of stress develop
tissues of low nutritional quality and palatability. A mangrove is an example of an
ecosystem with plant species that are characterized by sclerophyllous leaves, with
subepidermal layers with calcium oxalate crystals and high concentrations of Na (Lima
2013).
In addition to diverse defensive leaf attributes, mangroves are low in plant
diversity and have the lowest diversity of resources for insects compared to other
vegetation formations. The woody flora of the mangrove in Babitonga Bay (Santa
Catarina, Brazil), for example, comprises only Laguncularia racemosa (L.) C.F. Gaertn.,
Rhizophora mangle (Rhizophoraceae) L. and Avicennia schaueriana (Verbenaceae) Stapf
& Leechm. ex Moldenke (Kilca et al. 2011).
The average herbivory rate recorded in mangroves is around 10% (Menezes &
Peixoto 2009); miners are the most common type of herbivore, followed by gallers and
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chewers (Menezes & Peixoto 2009). Among arboreal mangrove species, those of the
genus Avicennia suffer major damage from herbivory and have the highest diversity of
associated insect feeding guilds (Kathiresan 2003; Menezes & Peixoto 2009).
Unlike the records of plant-herbivore interaction mentioned above, some insects
can cause intense damage to plants by consuming massive amounts of plant tissue,
resulting in direct and indirect physiological and ecological damage to the plant resource.
For example, Hyblaea puera Cramer (Lepidoptera: Hyblaeidae) consumes the entire
canopy of Tectona grandis in India and Mexico (Nair 2007; Cibrián-Llanderal 2015),
resulting in important economic losses (Nair 2007). Recently, H. puera was registered in
India causing severe and extensive damage to mangrove communities (Arun & Mahajan
2012). Similarly, the massive consumption of mangroves by H. puera was reported in
Brazil in the states of Pará (Menezes & Mehlig 2005, 2008; Fernandes et al. 2009), Rio
de Janeiro (Menezes & Peixoto 2009), Paraná (Faraco et al. 2019) and Santa Catarina
(Melo Jr. et al. 2017).
Although the caterpillar of H. puera attacks all mangrove species, mass
consumption occurs only in Aviccenia species in all studied locations (Menezes & Mehlig
2005, 2208; Fernandes et al. 2009; Menezes & Peixoto 2009; Arun & Mahajan 2012;
Faraco et al. 2019). With respect to mangrove herbivory, Fernandes et al. (2009) showed
evidence that mass herbivory by H. puera causes an increase in nutrient cycling in the
soil and, consequently, increases the productivity in aquatic ecosystems. However, no
study has evaluated the impact of herbivory by H. puera on the plant itself.
The impacts of herbivory on a plant community can be direct, such as changes in
leaf characteristics after the herbivory event and death of the plant specimen consumed
(Traw & Dawson 2002), and indirect, such as changes in the plant community structure
(Norghauer & Newbery, 2014) and changes in the network of insect-plant interactions
(e.g., herbivory interaction or pollination) (Glaum & Kessler 2017; Santangelo et al.
2018).
The objective of the present study was to evaluate the direct impact caused by the
massive herbivory of A. shaueriana leaves in Babitonga Bay. The hypothesis was that
after the herbivory event A. schaueriana would exhibit leaf morphoanatomical changes.
We predicted that leaves in the affected mangrove would possess more marked anti-
herbivory attributes (more sclerophyllous leaves with lower water content and greater
distribution of secondary metabolites) in relation to leaves in a non-affected mangrove.
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2 MATERIAL AND METHODS
The study was conducted between February and March 2018 in an area of
mangrove forest in the municipality of Joinville (26°17'09.8"S, 48°47'05.4"W; -
26.286068, -48.784824), in the northeastern region of the state of Santa Catarina. The
climate of the region falls within the humid climate zone and is predominantly humid
mesothermic with hot summers (Cfa of Köeppen). Rainfall is well distributed throughout
the year with common south winds bringing oceanic humidity to the atmosphere that
results in wet winters. The mean annual temperature is 20.6 °C.
The mangrove is associated with Babitonga Bay, which together form the largest
estuary in the region (Xavier and Maia, 2008, Kilca et al. 2011). The mangrove cover in
the city of Joinville corresponds to 76% of the mangroves in Santa Catarina State
(Babitonga Ativa unpublished data).
Avicennia schaueriana was selected for the study because it is the taxon most
attacked by insects, including Hyblaea puera (Menezes & Mehlig 2005, 2208; Fernandes
et al. 2009; Menezes & Peixoto 2009; Arun & Mahajan 2012; Faraco et al. 2019).
Popularly known as black mangrove, A. schaueriana is a tree characterized by its smooth,
light brown bark, fine, long pneumatophores, and light green leaves with a rounded apex
and glands throughout the epidermis (Silva et al. 2010).
The material collected came from plants that sprouted after an herbivory attack by
H. puera (around two months after the herbivory event) and the control corresponds to a
population of A. schaueriana that had not suffered an attack by insects, which is located
around 2 km from the attacked population. In the location that was attacked by H. puera
the canopies of the individuals of A. schaueriana were completely consumed, which
killed the main branches of the trees, leaving only trunks, and sometimes killed the
specimens.
Ten adult individuals of A. schaueriana with a DBH > 16 cm, which resprouted
after the herbivory event, were selected in the attacked area, and ten individuals were
selected in the control area near the border of Babitonga Bay. Forty-five completely
expanded leaves between the third and the fifth node from the branch apex were collected
from each individual. Twenty-five leaves per individual were weighed in the laboratory
on a precision analytical balance to obtain the fresh mass (g) and puncture force (N/mm²),
which was measured with a digital penetrometer (MOD. PTR-300, Instrutherm)
(Cornelissen & Stiling 2006) using a size 1 entomological pin (40 x 0.30 mm) as the
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piercing instrument. The leaves were then oven dried at 70ºC and weighed, again with a
precision analytical balance, to obtain the dry mass (g). Leaf water content (g) was
determined as the difference between fresh and dry mass. Leaf area (cm²) was measured
using an image obtained from a table scanner, calculated using the software Sigma Scan
Pro 5.0, and the leaf area consumed by the herbivores was calculated as (complete area -
remaining leaf area). The specific leaf area (SLA, g/cm²) values were then calculated from
the ratio between leaf area and dry mass (Pérez-Harguindeguy et al. 2013).
For the leaf nutrition analysis (nitrogen content), five mature leaves of each
individual were ground in a ball mill. The content was sieved in a 0.25 mm granulometric
sieve and analyzed in an elemental analyzer. Three composite samples were produced for
each collection point. The analysis was performed using the combustion method (Nelson
and Sommers 1996).
Histochemical characterization was performed with five leaves, which were fixed
in FAA (formaldehyde, acetic acid and 70% alcohol) in the field and preserved in 70%
alcohol. Freehand cuts were made with the aid of a steel knife in the middle third of the
leaf and close to the central vein. The cuts were tested for the presence of tannins using
2% hydrochloric vanillin, phenolics with ferric chloride, lignin with floroglucionol and
alkaloids with Dragendorf reagent. Semi-permanent slides were then assembled of the
reactions. White tests were performed on each slide.
Means and standard deviations were calculated for all leaf attributes. The
normality of the attributes was tested using the Shapiro-Wilk test and the homogeneity of
the variances by the Levene test. Means were compared using the Wilcoxon test of
independent samples with alfa= 0.05. The statistical analyses were performed in the R
environment, version 3.6.1 (Borcard et al. 2011).
3 RESULTS
The statistical analyses indicated that the leaf attributes evaluated did not have a
normal distribution (pBrazilian Journal of Development 47280
ISSN: 2525-8761
marginally significant difference, but nutritional quality did not differ between this area
and the control mangrove (Tab. 1).
A qualitative analysis of the presence of secondary metabolites revealed a greater
distribution of phenolic compounds and alkaloids in the leaf tissue of A. schaueriana from
the population in the regenerating area. Tannins were not observed in the mesophyll of
leaves from either population (Tab. 2).
Table 1. Means and standard deviations for the leaf attributes of Avicennia schaueriana from two
mangrove areas in Babitonga Bay, Joinville, Santa Catarina, Brazil. Legend: Values in black
indicate a statistically significant (α ≤ 0.05) difference for the attribute.
Attributes Regenerating Control P
Specific leaf area (g/cm³) 46.19 (5.13) 60.01 (9.88)Brazilian Journal of Development 47281
ISSN: 2525-8761
compared to Rhizophora mangle L. (Rhizophoraceae) and Laguncularia racemosa (L.)
C.F. Gaertn (Godoy et al. 1997; Lima et al. 2013). The nutritional value of plant tissue is
determined by a combination of characteristics, such as the following: amount of fibers,
which directly influences leaf hardness and palatability; amount of water; and nitrogen
content (Caldwell et al. 2016). Nitrogen plays an important role in the biosynthesis of
proteins and chlorophyll, in addition to delaying the lignification of tissues (Deuner et al
2008, Caixeta et al. 2004). For the herbivore, on the other hand, this nutrient is important
for the synthesis of proteins and their amino acids (Caixeta et al. 2004), and thus
represents an important factor in the choice of plant tissue by the herbivore. In this sense,
the species studied has a higher amount of nitrogen and less leaf sclerophylly compared
to the other species (Lima et al. 2013).
The leaves in the regenerating area had lower SLA, making the mesophyll harder
and therefore less palatable (Coley 1983), as well as lower water content, which
represents lower nutritional quality. Thus, the energetic cost of consuming this vegetal
tissue, combined with its low nutritional quality, makes it an unviable resource for the
herbivore, resulting in decreased rates of herbivory (Caldwell et al. 2016).
The force needed to perforate, cut or break a leaf is an important predictor of
resistance against herbivory (Caldwell et al. 2016). Although “hardness” has been
frequently characterized as physical, it can result from different pathways, such as the
deposition of chemical compounds in different leaf tissues (e.g., lignin, cellulose, silica).
Intuitively, it was expected that leaves with more fibers would require more force to be
perforated. However, the opposite was observed, which may be the result of attributes not
evaluated in the present study, such as leaf blade thickness that can make it difficult for
insects to consume this plant material.
When associating all the nutritional leaf attributes, the plants in the control area
were more palatable (greater AEF) and had higher nutritional quality (greater water
content), as well as high levels of N in relation to the other species of this ecosystem
(Serenesky et al. 2013). However, in contrast, the leaves in this area were harder
(puncture force). Kunikichi & Masashi (2012) evaluated the effect of leaf hardness of ten
plant species on 30 species of larvae in the family Notodontidae (Lepidoptera) and
demonstrated a positive relationship between leaf hardness and body size and
characteristics of the head and mandibles of the larvae. Thus, even though they are harder,
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the leaves in the control area can be more nutritious and preferred by the insects since
they induce greater growth of larvae.
In combination with the morphological attributes, secondary metabolites comprise
an important source of plant defenses against insects. They are chemical compounds with
non-vital functions that are produced by the plant metabolism. They compose a wide
range of compounds of varying composition, and can act as repellents against herbivorous
insects by causing an immediate effect on herbivory (compounds with astringent taste) or
affects after consumption (compounds that affect the nervous system or processes of
development and reproduction of insect herbivores) (Lattanzio et al. 2006; War et al.
2012). Alkaloids, for example, can dramatically reduce herbivore plant preference (Macel
et al. 2010; Shields et al. 2008), since they affect the growth and development of insects
leading to death (Levinson 1976).
Phenolic compounds are a class of metabolites of great diversity and distribution
in the plant kingdom (Kubalt 2016), and play fundamental roles in several physiological
processes, as well as in defense against herbivory and pathogens (Lattanzio et al. 2006).
As an anti-herbivory defense, phenolic compounds may have a bitter or astringent taste
in plant tissues or influence leaf hardness due to the presence of lignin, characteristics
that act immediately upon consumption. On the other hand, phenolic compounds may act
later in the processes of development and reproduction of herbivores, resulting in failures
in cellular and metabolic processes (Ramalho & Silva 2010). Both compounds evaluated,
alkaloids and phenolic compounds, were present in more leaf tissues of the regenerating
plants than the leaves of plants in the control environment.
In addition, unlike R. mangle and L. racemosa, A. schaueriana does not have
tannins in its leaf tissues. Tannins are the most common metabolites produced in plants,
corresponding to around 5 to 10% of the dry weight of leaves, and can be toxic to insects
(Barbehenn & constabel 2011). Thus, the absence of these metabolites can influence the
preference of insects in relation to other species. In evolutionary history, the transition of
the Rosidae-Asteridae subclasses resulted in the absence of tannins in A. schaueriana
(Asteridae) and the presence of tannins in other mangrove species, such as L. racemosa
and R. mangle (Rosidae) (Godoy et al., 1997).
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