Infestation of Mangroves by the Invasive Moth Hyblaea puera (Cramer, 1777)(Lepidoptera: Hyblaeidae)

Abstract

We report the first known infestation of mangroves by the invasive moth Hyblaea puera in Paraná, Southern Brazil. The infestation caused massive defoliation of Avicennia schaueriana trees, affecting approximately 20,000 hectares of mangroves. We discuss the implications for conservation and management, focusing on protected areas, the ecology of mangroves, and local livelihoods.

Keywords:
pest quarantine; ecosystem services; insect-plant interactions; leaf consumption; litterfall.

INTRODUCTION

The teak defoliator moth Hyblaea puera (Cramer, 1777) (Lepidoptera: Hyblaeidae) is an invasive pest species [¹,²] known to attack commercial teak (Tectona grandis L.f Lamiaceae) plantations and cause extensive damage [³,⁴]. Teak has been exploited in Brazil since 1925 [⁵]; the first commercial plantations started in the 1960’s [⁶-⁸] and, by 2015, covered an estimated area of 87.4 K ha [⁹]. Despite its long history of commercial exploitation in Brazil, the first record of the teak defoliator moth in a commercial plantation did not occur until 1997, when an outbreak occurred in the State of Mato Grosso, in the west of the country [²,¹⁰,¹¹]. Besides teak, the teak defoliator moth has been recorded on 45 other host tree species [²,¹²-¹⁴]. Among these other host species, the moth has been found on black mangroves (Avicennia sp.), and there is strong evidence that it has adapted its life-history traits to suit the micro-environmental conditions of the mangrove ecosystem [¹⁵].

In general, herbivory in mangrove forests is a minor route for organic matter transfer, and insect herbivores typically only cause moderate damage (not exceeding 5% of the leaf area) [¹⁶-¹⁸]. To date, there have been few studies of mangrove herbivory that have provided detailed information on the consequences of defoliation events [¹⁹-²³]. Nevertheless, there is evidence that heavy defoliation caused by insects can negatively affect reproduction of mangrove trees [¹⁹], making invasion by the teak defoliator moth a major concern for this already threatened ecosystem. These fears have recently been realized, with reports of the teak defoliator moth causing severe and extensive defoliation of Avicennia trees in geographically dispersed mangrove forests on the Brazilian coast. The first report was from Pará state, northern Brazil (1°03’26”S, 46°45’45”W) where a severe defoliation of A. germinans (L.) L. was described [²⁴-²⁶]. Menezes and Peixoto [²⁷] have also reported widespread defoliation and necrosis of Avicennia schaueriana Stapf & Leechman ex Moldenke trees in Rio de Janeiro State due to a H. puera population explosion.

In Paraná State (southern Brazil), mangroves cover around 30,800 ha of the coastline, being the predominant intertidal ecosystem around two estuarine systems: the Paranaguá Estuarine Complex and Guaratuba Bay (Fig. 1). Mangrove forests in this region are composed of three tree species: Rhizophora mangle L., Laguncularia racemosa (L.) C.F. Gaertn. and A. schaueriana. Most of these forests are protected by a variety of sustainable use and no-take protected areas, an indication of the overall importance of this ecosystem for biodiversity conservation. Indeed, the mangroves are contiguous with one of the largest remaining sections of the Atlantic Rainforest Biome, a global biodiversity hotspot (28).

Figure 1
Intensity of infection by H. puera in mangroves of Paraná in 2016.

MATERIAL AND METHODS

The onset of the Paraná infestation was first noticed by local fishermen, who reported, in February 2016, massive black mangrove defoliation to the Chico Mendes Institute for Biodiversity Conservation (ICMBio), responsible for management of federal protected areas. In Santa Catarina state (adjoining Paraná), an infestation was reported by representatives of Joinville municipality, who sent samples of adult moths to the Federal University of Paraná, also in February.

Between March and May 2016, we observed the consequences of the infestation and collected data on the distribution of A. schaueriana defoliation, as a direct indicator of the occurrence of the moth. During boat surveys, we observed massive and widespread defoliation of A. schaueriana trees, and collected larvae and pupae from infected trees. Most individuals of A. schaueriana were completely defoliated, though no infestation was observed on the other two mangrove species. Identification of H. puera was confirmed by the Laboratório de Estudos de Lepidoptera Neotropical (Universidade Federal do Paraná, Zoology Department). Two adults and two pupae were deposited as vouchers in the Coleção Entomológica Padre Jesus Santiago Moure (DZUP).

On April 20, 2016, an aerial survey of the coast of Paraná and northern coast of Santa Catarina was conducted using a helicopter. We registered visual observations of defoliation in a GIS and estimated the size of the affected area. Intensity of the attack (high, medium, and low) was based on visual observation of the density of defoliated trees in each area. We evaluated the impact of the herbivory on mangroves, focusing on protected areas within Paraná State (Table 1).

Table 1
Impact of the herbivory of the moth H. puera on A. schaueriana in Federal and State protected areas during the outbreak of 2016 in Paraná State, Brazil.

	Protected area	affected area (ha)1	Total PA area (ha)	% affected area
State level	Boguaçu State Park	1150.6	6660.8	17.3
	Guaraqueçaba State EPA2	8011.0	231802.2	3.5
	Guaratuba State EPA	5605.5	199455.2	2.8
National level	Guaraqueçaba Ecological Station	3294.4	4370.1	75.4
	Bom Jesus Biological Reserve	478.5	34179.0	1.4
	Superagui National Park	663.8	33860.6	2.0
	Guaraqueçaba Federal EPA	11054.6	282446.3	3.9

• 1. Some of these protected areas are zoned, with no-take PAs inside sustainable use areas. Therefore, the sum of affected areas in Table 1 is larger than the total affected area showed in Table 2.
• 2. EPA = Environmental Protection Area; a type of sustainable use protected area equivalent to IUCN Category VI. The other cited protected areas are no-take, equivalent to IUCN Categories Ia, Ib and II.

RESULTS

An estimated 20,357.93 hectares of mangrove forest were affected at different levels according to the density of Avicennia trees and, possibly, to proximity to urban and harbor areas (Table 2 and Figure 1). This represents 66% of the total area of mangroves in Paraná. Two protected areas were particularly affected: the Guaraqueçaba Ecological Station (75.39% of area affected) and Boguaçu State Park (17.27% affected).

Table 2
Qualitative impact level of the moth H. puera on A. schaueriana during the outbreak of 2016 in Paraná State, Brazil.

Attack intensity	Affected area (ha)	Total mangrove area (ha)	%
Low	2262.9	30884.4	7.3
Medium	14433.2		46.7
High	3661.8		11.9
total	20357.9		65.9

In June 2016, we revisited some of the infected areas and observed that most trees showed signs of recovery, with budding leaves. No dead trees were observed. We also found some empty puparia but no signs of larvae.

DISCUSSION

Although measured under different environmental conditions, a study in Pernambuco State in tropical northeast Brazil reported a leaf formation rate of 48 days with a leaf life span of 13.1 months for healthy A. schaueriana [²⁹]. This suggests that there may be a slower rate of leaf formation in infected sites, though further investigation is required to confirm this. Our observations corroborate others on northern populations of A. germinans [²⁴,²⁵,26]. Fernandes et al. [²⁶] reported that H. puera larvae were able to deplete both young and senescent leaves within a short period of time, with a few trees not surviving the attack.

The outbreak in Paraná state occurred in synchrony with outbreaks in Santos (São Paulo State) and Joinville (Santa Catarina State). These regions host some of the largest and busiest ports in Brazil. Port regions have been implicated in the introduction of moth species in other parts of the world. For example, ship structures and cargos with egg masses of the gypsy moth Lymantria dispar L. (Lepidoptera: Noctuidae: Lymantriinae) have been noted on more than one occasion in North America [³⁰]. Moth larvae have also been observed ‘ballooning’ from a superstructure and being carried downwind toward the shore [³⁰]. Therefore, despite assumptions that the teak moth was introduced with teak vegetative material, it is possible that ports have also contributed to the entry of new genetic material of H. puera into Brazil. Nonetheless, we cannot discard the hypothesis that teak plantations have played an important role in the infestation of mangroves by the teak defoliator moth. In this context, a genetic survey could potentially identify the invasion routes of the moth.

The introduction and spread of an invasive pest species inevitably raises concerns about ecological impacts. In the current example, herbivory by H. puera on Avicennia may influence energy transfer in the system. The moth infestation converts Avicennia leaves into particulate organic matter over a short period of time, favoring nutrient cycling in the mangroves and providing a nutrient supply for neighboring aquatic systems [²⁶]. This can have short-term impacts, increasing secondary production and local fish catches [²⁵,²⁶]. Nevertheless, overall negative impacts on mangrove health are expected, especially if new outbreaks occur in short periods of time.

The creation of a permanent observation and monitoring area for this ecosystem is currently under discussion by state and federal research and management institutions, and we will continue to observe the impact of these infestations. A biannual pattern of moth outbreaks has been reported in Brazil and other countries [²⁶], but, as late as June 2019, no new occurrences have been observed in the region. Attention should be especially focused on protected areas and on the possible impacts of moth outbreaks on the wider ecology of mangroves and estuaries. There may also be consequences for the livelihoods of local fishers, some of whom rely heavily on mangrove crabs and oysters as a supplementary source of income and food [³¹].

Acknowledgments:

We would like to thank ICMBio and IAP/SEMA for transport in field trips, and Professor Mirna Casagrande, Department of Zoology/UFPR, for identification of adults and larvae of H. puera.

REFERENCES

• ¹
  Varma R. Invasive alien species of weeds and insects: the agriculture-forestry nexus, examples from India. Asia-Pacific Forest Invasive Species Network Workshop 22-25 February 2005, Ho Chi Minh City, Viet Nam. Bangkok, 2007.
• ²
  Peres-Filho, O.; Dorval, A.; Berti-Filho, E. Ocorrência de Hyblaea puera (CRAMER, 1777) (LEPIDOPTERA: HYBLAEIDAE) em teca no Brasil. Bragantia. 2002, 61(1), 59-60.
• ³
  Cibrián-Llanderal, V.; González-Hernandez, H.; Cibrián-Tovar, D.; Campos-Figueroa, M.; de los Santos-Posadas, H.; Rodríguez-Maciel, J. et al. Incidence of Hyblaea puera (Lepidoptera : Hyblaeidae) in Mexico. Southwest Entomol [Internet]. 2015, 40(2), 441-4. Available online: http://www.bioone.org/doi/full/10.3958/059.040.0220
  » http://www.bioone.org/doi/full/10.3958/059.040.0220
• ⁴
  Javaregowda, K.N.L. Seasonal incidence of Teak Defoliator, Hyblaea puera Cramer (Hyblaeidae: Lepidoptera) in Uttara Kannada District of Karnataka. Karnataka J Agric Sci. 2007, 20(1),153-4.
• ⁵
  Sampaio, A.J. A teca da Índia e a do Brasil. Rev Floresta. 1930, 1(9), 7-10.
• ⁶
  Schuhli, G.S.; Paludzyszyn Filho, E. O cenário da silvicultura de teca e perspectivas para o melhoramento genético. Pesqui Florest Bras. 2010, 30(63), 217-30.
• ⁷
  Delgado, L.G.M; Gomes, J.E.; Araujo, H.B. Análise do sistema de produção de teca (Tectona grandis L.f.) no Brasil. Rev científica eletrônica Eng Florest. 2008, 11,1-6.
• ⁸
  Figueiredo, E.O. Reflorestamento com teca (Tectona grandis L.F.) no Estado do Acre. [Internet]. Embrapa Acre: Rio Branco, Brasil, 2001; p. 28. Available online: https://www.embrapa.br/busca-de-publicacoes/-/publicacao/495886/reflorestamento-com-teca-tectona-grandis-l-f-no-estado-do-acre
  » https://www.embrapa.br/busca-de-publicacoes/-/publicacao/495886/reflorestamento-com-teca-tectona-grandis-l-f-no-estado-do-acre
• ⁹
  IBÁ. Relatório Anual. Brazilian Tree Ind. 2016, 53(9), 100.
• ¹⁰
  Ferreira, R.A.; Tosta, W.F.G.; Giacometti, V.G.; Souza, G.O.; Silva, J.M.S. Entomofauna observada na cultura da teca (Tectona grandis L.f), no campo. Rev Científica Eletrônica Eng Florest. 2009,14, 24 p.
• ¹¹
  Figueiredo, E.O.; Oliveira, L.C.; Barbosa, L.K.F. Teca (Tectona grandis L.f.): principais perguntas do futuro empreendedor florestal. Embrapa Acre: Rio Branco, Brasil, 2005; p. 87.
• ¹²
  Nair, K.S.S. Tropical forest insect pests: ecology, impact and management. Cambridge University Press: New York, USA, 2007; 404 p.
• ¹³
  Mohanadas, K. A new host record for the teak defoliator, Hyblaea puera (Lepidoptera, Hyblaeidae). Curr Sci. 1986, 55(23),1207-8.
• ¹⁴
  Baksha, M.W.; Crawley, M.J. Relative preference of different host plants to teak defoliator, Hyblaea puera Cram.(Hyblaeidae: Lepidoptera) in Bangladesh. Bangladesh J For Sci. 1995, 24, 21-5.
• ¹⁵
  Arun, P.R.; Mahajan, M.V. Ecological costs and benefits of Teak Defoliator (Hyblaea puera Cramer) outbreaks in a mangrove ecosystem. Marine Sci. 2012, 2(5), 48-51.
• ¹⁶
  Erickson, A.A.; Bell, S.S.; Dawes, C.J. Does mangrove leaf chemistry help explain crab herbivory patterns? Biotropica. 2004, 36, 333-43.
• ¹⁷
  Faraco, L.F.D.; Da Cunha Lana, P. Leaf-consumption levels in subtropical mangroves of Paranágua Bay (SE Brazil). Wetl Ecol Manag. 2004, 12(2), 115-22.
• ¹⁸
  Offenberg, J.; Havanon, S. Observations on the ecology of Weaver Ants (Oecophylla smaragdina Fabricius) in a Thai mangrove ecosystem and their effect on herbivory of Rhizophora mucronata Lam. Biotropica [Internet]. 2004, 36(3), 344-51. Available online: http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7429.2004.tb00326.x/abstract
  » http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7429.2004.tb00326.x/abstract
• ¹⁹
  Anderson, C.; Lee, S.Y. Defoliation of the mangrove Avicennia marina in Hong Kong : Cause and consequences. Biotropica. 1995, 27(2), 218-26.
• ²⁰
  Burrows, D.W. The role of insect leaf herbivory on the mangroves Avicennia marina and Rhizophora stylosa. PhD Thesis, James Cook University, 2003.
• ²¹
  Duke, N.C. Sustained high levels of foliar herbivory of the mangrove Rhizophora stylosa by a moth larva Doratifera stenosa (Limacodidae) in north-eastern Australia. Wetl Ecol Manag. 2002, 10(5): 403-19.
• ²²
  Gara, R.I.; Sarango, A.; Cannon, P.G. Defoliation of an Ecuadorian mangrove forest by the bagworm, Oiketicus kirbyi Guilding (Lepidoptera: Psychidae). J Trop For Sci [Internet]. Forest Research Institute Malaysia 1990, 3(2), 181-6. Available online: http://www.jstor.org/stable/43594383
  » http://www.jstor.org/stable/43594383
• ²³
  Tong, Y.F.; Lee, S.Y.; Morton, B. The herbivore assemblage, herbivory and leaf chemistry of the mangrove Kandelia obovata in two contrasting forests in Hong Kong. Wetl Ecol Manag. 2006, 14(1), 39-52.
• ²⁴
  Mehlig, U.; Menezes, M.P.M. Mass defoliation of the Mangrove Tree Avicennia germinans by the moth Hyblaea puera (Lepidoptera: Hyblaeidae) in Equatorial Brazil. Ecotropica. 2005, 11(1999), 87-8.
• ²⁵
  Menezes, M.P.M.; Mehlig, U. Desfolhação Maciça de Árvores de Avicennia germinans (L.) Stearn 1958 (Avicenniaceae) por Hyblaea puera (Lepidoptera : Hyblaeidae), nos Manguezais da Península de Bragança , Pará, Brasil. Bol do Mus Para Emílio Goeldi. 2005, 1958, 221-6.
• ²⁶
  Fernandes, M.E.B.; Nascimento, A.A.M.; Carvalho, M.L. Effects of herbivory by Hyblaea puera (Hyblaeidae: Lepidoptera) on litter production in the mangrove on the coast of Brazilian Amazonia. J Trop Ecol [Internet]. 2009, 25(3), 337. Available online: http://www.journals.cambridge.org/abstract_S0266467409005884
  » http://www.journals.cambridge.org/abstract_S0266467409005884
• ²⁷
  Menezes, L.F.T.; Peixoto, A.L. Leaf damage in a mangrove swamp at Sepetiba Bay, Rio de Janeiro, Brazil. Rev Bras Botânica. 2009, 32(4),715-24.
• ²⁸
  Myers, N.; Mittermeier, R.A.; Mittermeier, C.G.B.; Da Fonseca, G.A.B; Kent, J. Biodiversity hotspots for conservation priorities. Nature 2000, 403, 853-8.
• ²⁹
  Medeiros, T.C.C.; Sampaio, E.V.S.B. Leaf and flower formation in shoot tips of mangrove trees in Pernambuco, Brazil. Wetl Ecol Manag. 2013, 21(3), 209-17.
• ³⁰
  Bogdanowicz, S.M.; Wallner, W.E.; Bell, J.; Odell, T.M.; Harrison, R.G. Asian Gypsy Moths (Lepidoptera: Lymantriidae) in North America : evidence from molecular data. Ann Entomol Soc Am. 1993, 86(6), 710-5.
• ³¹
  Faraco, L.F.D.; Andriguetto-Filho, J.M.; Daw, T.M.; Lana, P.C.; Teixeira, C.F. Vulnerability among fishers in southern Brazil and its relation to Marine Protected Areas in a scenario of declining fisheries. Desenvolv Meio Ambiente 2016, 38, 51-76.

• Funding:

  This research received no external funding.

HIGHLIGHTS

• 3
  We report the first known infestation by Hyblaea puera in mangroves of Paraná, Southern Brazil.
• 4
  Massive defoliation of Avicennia schaueriana was observed in a large portion of local mangroves.
• 5
  We visually estimated levels of impact, focusing on protected areas.

Publication Dates

• Publication in this collection
  24 Oct 2019
• Date of issue
  2019

History

• Received
  15 Aug 2017
• Accepted
  12 June 2019