The effect of seed ingestion by a native, generalist bird on the germination of worldwide potentially invasive trees species Pittosporum undulatum and Schinus terebinthifolia
Introduction
Invasive alien species are recognized as the second leading cause of biodiversity loss and species extinction worldwide (Bellard et al., 2016; Pyšek et al., 2017). In addition to the different ecological impacts (i.e. changes in ecological processes - Vitousek, 1990; Ewe and Sternberg, 2002; hybridization with similar species - Mesgaran et al., 2016; suppression of populations of native species - Chornesky and Randall, 2003; Donnelly et al., 2008), several invasive species cause a high economic and social impact (Pimentel et al., 2005; Holmes et al., 2009; Senator and Rozenberg, 2017), and may pose a serious risk to food security in communities or developing countries (GISP, 2007).
Australian cheesewood (Pittosporum undulatum Vent.) (Pittosporaceae) is a native Australian species and an alien species in Brazil, Mexico, Jamaica, South Africa, Portugal (Azores and Madeira Islands) and the United States (Lourenço et al., 2011; Bellingham et al., 2018). It is mainly present in the south and southeast in Brazil, appearing on the list of invasive species of all states in the southern region (Negrelle et al., 2018), being the second most frequent invasive species in Conservation Units in the State of Paraná (Mielke et al., 2010). The species is considered ornamental due to its fragrant flowers, its showy and abundant crown and prolonged fruiting (Negrelle et al., 2018). The fruits are capsular, bivalve, dehiscent, and have an orange color, and they expose their seeds covered by a colorless, viscous and quite odorous resin when ripe.
Brazilian pepper (Schinus terebnthifolia Raddi) (Anacardiaceae) is a tree species with wide distribution in South America, occurring in a large part of the Brazilian territory, more abundantly in the Southeast and South regions (Carvalho, 2003; Flora do Brasil, http://www.floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB15471), and is one of the “100 World's Worst Invaders” (Lowe et al., 2000). It is considered an invasive species in approximately 20 countries in North and Central America, Oceania and Africa (CABI, https://www.cabi.org/isc/datasheet/49031). The species was originally introduced in the United States of America as ornamental in different locations (i.e. Florida, Hawaii) in the middle of the 19th century, becoming an important environmental and economic problem with more than US$3 million spent annually on chemical control of the species in Florida (Hiatt et al., 2019). In addition to the ornamental potential, its reddish and bright colored fruits have cosmetic, pharmaceutical, and medicinal properties when ripe, and can be used as a condiment in human food (Silva et al., 2017). As a result, its use has been spread around the world, which can expand the problem to other regions of the planet. Similar to P. undulatum, the seeds are covered by a sticky and aromatic resin, which in turn has an amber color (Carmello-Guerreiro and Paoli, 2002).
Both tree species present high productivity of fruit and seeds annually which are ingested by many bird species, especially those of the Passeriformes, which disperse the seeds, in turn leading to effects on germination (Campagnoli et al., 2016; D'Avila et al., 2010; Dlamini et al., 2018; Gleadow, 1982; Vissoto et al., 2019). Thus, these species play an important food resource for birds in their naturally occurring areas and have a fundamental role in restoring forest environments. However, these same characteristics make them so aggressive in occupying new environments where they were introduced, since introduced exotic plants can contribute to the diet of native frugivorous animals which are in charge of their dispersion (Mokotjomela et al., 2013; Ortega-Flores et al., 2018).
Frugivorous animals play an important role for the dispersion and establishment of zoochoric plant species (Bascompte and Jordano, 2007; Vissoto et al., 2019). According to Howe and Smallwood (1982), the zoochoric dispersion syndrome by birds and mammals represents 50–75% of adapted plants in tropical forests, and approximately one third of tropical bird species are frugivorous (Snow, 1981). The Great Kiskadee (Pitangus sulphuratus) is a bird with wide distribution in Latin America, occurring from Mexico to Argentina, and is a migratory species in the United States and Uruguay. It occurs in practically all regions in Brazil, being expressively abundant in the South and Southeast. It is considered a generalist because it inhabits several types of environments, including degraded and urban areas, in addition to having an omnivorous diet mainly based on fruits and small arthropods (Sick, 1997; Mobley, 2020).
The zoochoric dispersion of invasive plants is an important area for their management, and information about how these disperser animals affect their propagation and establishment should be researched (Buckley et al., 2006). However, a topic which is constantly discussed and still controversial in studies involving different native and exotic animal and vegetable species is the influence on germination due to the passage of seeds through the digestive tract of different dispersers, which may have a positive, negative or indifferent effect (Traveset, 1998; Ferreira et al., 2017). Nonetheless, different studies demonstrate that interactions between plant alien species and native birds do not improve seed germination, and they are only effective for its dispersion (Barnea et al., 1990; Jordaan and Downs, 2012; Jordaan et al., 2011a, 2011b).
Some aspects considered as germination enhancers are the mechanical and chemical scarification resulting from processes such as the mandibulation and action of digestive acids, mainly related to overcoming integumentary numbness (Barnea et al., 1991; Traveset, 1998). Substances often present in structures and compounds of fruits and seeds which inhibit germination can also be eliminated during the passage through the animal's digestive tract (Robertson et al., 2006). Such strategies which are common in zoochoric species would avoid intraspecific competition, thereby favoring the germination of only those seeds ingested and dispersed by the fauna away from the mother plant, leaving the seeds of those fruits which fall by gravity having less chance of germinating (Janzen, 1970). In view of the above, our objective was to evaluate the germinability of P. undulatum and S. terebinthifolia, with the prediction that ingestion of seeds and subsequent defecation by birds increases the germination of these species.
Section snippets
Study area
Our study was conducted at the Cascata Experimental Station (EEC) in Pelotas, Rio Grande do Sul State in southern Brazil, 160 m. a.s.l. The region's climate is defined as Cfa according to the Koppen classification, being a humid temperate climate with hot summers, without a dry season (Alvares et al., 2013), with an average temperature of 18.9 °C and an average rainfall of 1794.6 mm per year. The study area has approximately 0.35 ha of fields, previously covered by Semi-deciduous Seasonal
Results
Great Kiskadees (Pitangus sulphuratus) were observed visiting perches in all focal observation periods. The birds used the structures for landing and foraging, eventually defecating on the collectors, and up to four individuals of this species were sighted simultaneously using the structures. Another five species of birds were recorded using perches (Rupornis magnirostris, Furnarius rufus, Xolmis irupero, Sicalis flaveola and Pseudoleistes guirahuro), but only Great Kiskadees include fruit in
Discussion
We have shown that there is a positive effect on seed germination for both studied species caused by the ingestion by Great Kiskadees. Excreted P. undulatum seeds have a higher germination speed and percentage when compared to intact seeds, and the germinated seed rate over time also differed between treatments, showing superiority for seeds collected under artificial perches, a pattern which is also repeated for excreted S. terebinthifolia seeds. However, the positive germination effect for S.
Conclusions
Although the seed passage through the digestive tract of birds did not significantly alter the germination rates of S. terebinthifolia, Great Kiskadees are still an important seed germination enhancer of P. undulatum, enabling the colonization of new areas in the Southern Brazil Atlantic Forest. Therefore, the plant-frugivore is a species-specific interaction which varies between species. New works must be carried out with the objective of seeking information on plant-frugivore interactions,
Author contributions
GCG originally formulated the idea, GCG, TCF, ARM and ESGG developed the methodology GCG, TCF and conducted the fieldwork, ESGG and IMLR performed the statistical analyses, GCG, TCF, ARM, ESGG, IMLR and RB wrote the manuscript.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We would like to thank Embrapa Clima Temperado (proc. 04.16.05.006.00.00 Embrapa - RestauraSul), in particular the Management and Restoration of Native Vegetation group, the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; proc. 441575/2017–0) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001, for the logistical and financial support to carry out the work.
References (70)
- et al.
Endemic trees in a tropical biodiversity hotspot imperilled by an invasive tree
Biol. Conserv.
(2018) - et al.
The effect of frugivorous birds on seed dispersal and germination of the invasive Brazilian pepper tree (Schinus terebinthifolius) and Indian laurel (Litsea glutinosa)
South Afr. J. Bot.
(2018) - et al.
Allelopathic effects of fruits of the Brazilian pepper Schinus terebinthifolius on growth, leaf production and biomass of seedlings of the red mangrove Rhizophora mangle and the black mangrove Avicennia germinans
J. Exp. Mar. Biol. Ecol.
(2008) - et al.
Comparison of germination rates and fruit traits of indigenous Solanum giganteum and invasive S. mauritianum in South Africa
South Afr. J. Bot.
(2012) - et al.
Distribution, habitat and biomass of Pittosporum undulatum, the most important woody plant invader in the Azores Archipelago
For. Ecol. Manag.
(2011) - et al.
Is Solanum mauritianum a preferential food resource for native frugivores in the Cape Floristic Region?
South Afr. J. Bot.
(2009) - et al.
Frugivorous birds visit fruits of emerging alien shrub species more frequently than those of native shrub species in the South African Mediterranean climate region
South Afr. J. Bot.
(2013) - et al.
Natural inhibitors of germination and growth VI. detection of a carboxyterminal fragment of the heat shock protein hsp 70 after coumarin treatment
J. Plant Physiol.
(1992) - et al.
Update on the environmental and economic costs associated with alien-invasive species in the United States
Ecol. Econ.
(2005) Effect of seed passage through vertebrate frugivores' guts on germination: a review
Perspect. Plant Ecol. Evol. Systemat.
(1998)