The effect of seed ingestion by a native, generalist bird on the germination of worldwide potentially invasive trees species Pittosporum undulatum and Schinus terebinthifolia

Highlights

• The positive effect on germination was significant in the alien species seeds, and greater than in the native species.

• Pitangus sulphuratus is an important potential disperser for the germination of P. undulatum seeds.

• The novelty in using artificial perches as a method for obtaining seeds ingested by birds.

Abstract

Invasive alien species are recognized as the second leading cause of biodiversity loss and species extinction worldwide, with zoochoric dispersion being a key factor for the success of invasive organisms as they can favor the germination of these species. We performed a study in the southern Brazil involving three generalist species with abundant and wide amount of distribution in Latin America, with the objective of evaluating seed ingestion by positive criteria about its germination. We investigated the role of bird digestion on the germination of a native pioneer species, the Brazilian pepper—Schinus terebinthifolia, an invasive alien species in many parts of the world. We compared the germination of this native with those of the invasive Australian cheesewood (Pittosporum undulatum) concurrently. Interestingly, the effect of potentiating germination was more intense in the introduced species than for the native species. Pitangus sulphuratus is an important potential disperser for the germination of P. undulatum seeds, enabling the colonization of new areas in the Atlantic Forest of southern Brazil.

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.