Resurgence of Harrisia Portoricensis (Cactaceae) on Desecheo Island After the Removal of Invasive Vertebrates: Management Implications
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Vol. 34: 339–347, 2017 ENDANGERED SPECIES RESEARCH Published November 23 https://doi.org/10.3354/esr00860 Endang Species Res OPENPEN ACCESSCCESS Resurgence of Harrisia portoricensis (Cactaceae) on Desecheo Island after the removal of invasive vertebrates: management implications Cielo E. Figuerola-Hernández1,*, Kirsty Swinnerton1,2, Nick D. Holmes1, Omar A. Monsegur-Rivera3, José Luis Herrera-Giraldo1, Coral Wolf1,4, Chad Hanson1, Susan Silander5, Donald A. Croll4 1Island Conservation, Santa Cruz, California 95060, USA 2The Island Endemics Foundation, Boquerón 00622, Puerto Rico 3Caribbean Ecological Services Field Office, US Fish and Wildlife Service, Boquerón 00622, Puerto Rico 4Coastal Conservation Action Lab, University of California Santa Cruz, Santa Cruz, California 95060, USA 5Caribbean National Wildlife Refuge Complex, US Fish and Wildlife Service, Boquerón 00622, Puerto Rico ABSTRACT: Desecheo Island hosts a natural population of the higo chumbo cactus Harrisia por- toricensis, listed as threatened under the US Endangered Species Act. The species was extirpated from mainland Puerto Rico and is restricted to the offshore islands of Mona, Monito and Desecheo. Herbivory by goats Capra hircus, rhesus macaques Macaca mulatta, and black rats Rattus rattus introduced to Desecheo Island have likely contributed to a population decline, with only a few individuals of higo chumbo reported in 2003. As part of a restoration program, goats have been eradicated, macaques are considered functionally extirpated, and actions to remove invasive rodents were completed in 2016 and confirmed as successful in 2017. Systematic monitoring was implemented between 2010 and 2013, including widespread searches for H. portoricensis, collect- ing data on population structure, number of individuals, height, number of branches and evidence of phenological events. After 4 yr of continuous monitoring, 72 individual plants were identified, which exhibited increased height and branching throughout the study years. No seedlings were observed and only a few juveniles recorded, suggesting a resurgence from suppressed adults with limited recruitment. Long-term monitoring is critical to understanding the population dynamics of this species on Desecheo Island. Efforts to safeguard this species on the island require completion of the invasive vertebrate removals and would benefit from a seed banking program and manual establishment of new populations. KEY WORDS: Invasive species · Eradication · Threatened species · Caribbean · Herbivory · Harrisia portoricensis · Cactaceae · Desecheo Island INTRODUCTION crease plant diversity, alter plant community struc- ture, accelerate soil erosion, and aid seed dispersal of Islands represent key areas for biodiversity conser- exotic plants (Sussman & Tattersall 1981, Walter & vation due to high levels of species endemism (Myers Gillett 1998, Simberloff & Von Holle 1999, Rojas-San- et al. 2000). Invasive species have been identified as doval et al. 2014). The Caribbean is home to approxi - a leading cause of extinctions (Tershy et al. 2015), mately 11 000 plant species, of which 72% are and remain a primary threat to extant island biodi- endemic to the region (Anadón-Irizarry et al. 2012). versity (Wege et al. 2010). Insular flora face threats Within these, the Cactaceae family is one of the most from invasive herbivores and omnivores that de - vulnerable and ecologically important in the Carib- © C.E.F.-H., K.S., N.D.H., J.L.H.-G., C.W., C.H., D.A.C. and, out- *Corresponding author: side the USA, the US Government 2017. Open Access under [email protected] Creative Commons by Attribution Licence. Use, distribution and reproduction are un restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 340 Endang Species Res 34: 339–347, 2017 bean (Fleming & Valiente-Banuet 2002), containing a dation) as many seeds do not survive gut passage large number of endangered and threatened species (Shiels et al. 2013). Breckon & Kolterman (1994) esti- (Walter & Gillett 1998, Ortega-Baes & Godínez-Álvarez mated approxima tely 430 adult and 120 juvenile H. 2006). Threats include disturbance (Godí nez-Álvarez portoricensis in 1994; the presence of different sized et al. 2003), illegal collection and trade (Casas et al. individuals indicated that reproduction and recruit- 2002, Zimmermann & Pérez-Sandi 2006), habitat loss, ment were occurring. Subsequent observations have diseases and invasive species (USFWS 1996). suggested a dramatic decline, with 5 individuals re - The higo chumbo Harrisia portoricensis is a colum- corded in 1999 (Santiago-Vélez 2000) and 9 in 2003 nar cactus endemic to Puerto Rico and known only (Schwagerl pers. comm., cited in USFWS 2010), rep- from the offshore islands of Mona, Monito, and De - resenting 0.9 to 1.6% of the observations made in 1994. secheo, west of Puerto Rico (USFWS 1996). The spe- Conservation actions on Desecheo have included cies has been extirpated from the main island of re moval of macaques, goats, and rats. Attempts to re - Puerto Rico, and in 1990 it was listed as threatened move the macaques were initiated in 1977 (Evans under the US Endangered Species Act, and consid- 1989) with focused efforts between 1985 and 1987, ered Endangered under the 1997 IUCN Red List of and more recently since 2009. As of December 2013, Threatened Plants (Walter & Gillett 1998). Identified the population was considered functionally extinct, threats include natural catastrophes like hurricanes, i.e. reproduction ceased with only one wild macaque habitat modification, low genetic variation, and her- known to remain on the island, and as of 2017, the bivory by invasive species on Mona and Desecheo project was declared successful (Hanson et al. in islands (USFWS 1996). On Desecheo Island, rhesus press). Goat removal was initiated in 1976, with most macaques Macaca mulatta were introduced in 1966 individuals removed between 1998 and 2003 (USFWS (Evans 1989) and goats Capra hircus were introdu - unpubl. data); the last individuals were removed in ced through several undocumented events (Breckon 2009 (C. Hanson pers. obs.). In total, at least 642 goats et al. 1998, Meléndez-Ackerman et al. 2008). Black and 295 macaques were re moved (Evans 1989, rats Rattus rattus were introduced with the arrival of USFWS unpubl. data, Hanson in press). Rat eradica- the first Europeans into the region in the 15th century tion has been attempted twice: a failed attempt in (Woodbury et al. 1971). A total of 161 plant species 2012, and a second, successful attempt in 2016. The have been documented on Desecheo, and 59 of the removal of the herbivory pressure exerted by these total species were extirpated between 1915 and 1997 invasive species is expected to benefit native plant (Breckon 2000). The higo chumbo may have evolved populations, including H. portoricensis (USFWS 2011). in the presence of (now extinct) native browsers, but Point and baseline surveys for the higo chumbo was susceptible to in tense herbivory and frugivory were conducted in 2003 and 2009, respectively, but pressures exerted by introduced non-native goats, no individuals were found (Island Conservation 2009), macaques, and rats. Macaques have previously been although detection probability for seedlings and identified as detrimental to H. portoricensis, with juveniles could have been low due to their small size individuals observed breaking off and eating young (0 to 50 cm). Systematic monitoring was sub sequently stems (Noble & Meier 1989, Breckon 2000). Debris implemented from 2010 to 2013 and data on popula- from cactus foraging by macaques and goats was tion structure, architecture of individuals, and evi- reported by Evans (1989), including the consumption dence of phenological events were recorded. Here, of H. por toricensis fruits by macaques. Goats and we provide an updated report on the status of the macaques were observed feeding on the moist pulp population of H. portoricensis on Desecheo Island after heavy rains, suggesting this was an important following removal of invasive vertebrates, and make water source in the xeric climate on Desecheo (Evans recommendations for the management of the species. 1989). In addition to these negative impacts, macaques may have had a positive role as seed dispersers of H. portoricensis (e.g. Sengupta et al. 2014); however this MATERIALS AND METHODS is unclear. Black rat consumption of H. portoricensis is un known but should not be ruled out, given this Study site species is highly omnivorous, and fruit, seeds, and vegetative matter from plants constitute a frequent Desecheo is a small, mountainous island of 122 ha component of their diet (Shiels et al. 2013). However, (18° 23’ N, 67° 29’ W) approximately 21 km west of seed consumption by R. rattus when non-native on Punta Higüero, Puerto Rico. Maximum elevation is islands is generally a negative relationship (seed pre- 213 m (Morrison & Menzel 1972), and vegetation is a Figuerola-Hernández et al.: Cactus resurgence after invasive species removal 341 mosaic of grassy patches, shrublands, and woodlands alien species (Aslan et al. 2012), and it may now be with candelabra cacti and semi-deciduous forest relying on alternative mechanisms for pollination (Woodbury et al. 1971). Annual rainfall on Desecheo (Rojas-Sandoval 2010). On Mona Island, for exam- is 750 to 1039 mm (Morrison & Menzel 1972, Seiders ple, pollinators are known to include the hawkmoth et al. 1972), with a dry period from January to March