Island hopping in a biodiversity hotspotarchipelago: reconstructed invasion history andupdated status and distribution of alien frogs in
the Philippines
By Arman N. Pili*, Emerson Y. Sy, Mae Lowe L. Diesmos and Arvin C. Diesmos
AbstractSix alien frogs have been introduced in the Philippines: chronologically, Hylarana erythraea, Rhinella marina, Lithobates catesbeianus, Hoplobatrachus rugulosus, Kaloula pulchra, and Eleutherodactylus planirostris. Here, we collected and synthesized historical and geographical data to reconstruct their history of invasion and to update their current invasion status and distribution in the Philippines. Four pathway categories (falling in 8 subcategories) have facilitated their introduction: (1) intentional ‘release’ for biological control and hunting in the wild; (2) ‘escape’ from farms; (3) ‘contamination’ of agricultural commodities, fish stocks, and ornamental plants/nursery materials; and (4) ‘stowaway’ on container/bulk and (hitchhiker on) ship/boat – of which the last two were important in most recent introductions. The spatio-temporal pattern of distribution showed a stratified-diffusion process of spread involving primarily leading-edge and long-distance dispersal. The pathways that facilitated their secondary (post-introduction) long-distance dispersal were either the same as those of their introduction or shifted over time. Estimation of rate of spread showed that H. erythraea, R. marina, H. rugulosus, and K. pulchra have not reached spatial saturation and are conditioning to spread, with the latter spreading fastest. The status of Lithobates catesbeianus, whether it successfully established or not, is undetermined. Meanwhile, the other alien frogs are now considered fully invasive species, of which R. marina is the most widespread, whereas E. planirostris is the least distributed. Our study provides science-based information that can help guide the development and implementation of pathway-specific measures to prevent and control future and current invasions by alien frogs.
*Corresponding Author E-mail: [email protected]
Pacific Science, vol. 73, no. 3May 17, 2019 (Early view)
Introduction
The Philippines is the second-largest archipelago in the world (after Indonesia). It is
composed of more than 7,100 islands, of which about 2,000 are inhabited; 48 islands have a land
area greater than 90 km2 (hereafter, major islands). The Philippines forms part of the maritime
Southeast Asian Region and is located at the western fringes of the Pacific Ocean, extending to
the eastern boundary of the South China Sea, and northeastern boundary of the Sunda Shelf
(Diesmos et al. 2014). It is globally recognized as a megadiverse nation for its immensely rich
biodiversity (Heaney 1985, 1986; Heaney and Mittermeier 1997; Heaney et al. 1999). However,
it is also a global biodiversity conservation hotspot due to the ceaseless imperilment of its
biodiversity (Heaney et al. 1999, Myers et al. 2000). Major threats to its biodiversity include
habitat loss and deforestation, invasive alien species, emerging infectious diseases, and climate
change (Alcala et al. 2012, Brown et al. 2012a, Diesmos et al. 2014).
Invasive alien species are non-native species that cause ecological and evolutionary
changes which consequently impair different aspects of human socio-economic activities
(Pimentel et al. 2000, 2005, Clout and Williams 2009). They are major threats to global
biodiversity conservation (Secretariat of the Convention on Biological Diversity [CBD] 2015)
and are the primary cause of global contemporary animal extinctions (Clavero and Garcia-
Berthou 2005). To demonstrate the negative impacts of IAS, the invasion of alien frogs
(reviewed in Kraus 2015) have been implicated in diminishing native prey and predator species
(e.g., the cane toad [Rhinella marina] in Australia – Shine 2010; the American bullfrog
[Lithobates catesbeianus] in United States – Kiesecker et al. 2001; the African clawed frog
[Xenopus laevis] in France – Lafferty and Page 1997), shrinking geographic ranges of native
species (e.g., X. laevis in global invasive range – Measey et al. 2012), and transmitting parasites
and diseases to native species (e.g., amphibian Chytridomycosis – Fisher et al. 2009; amphibian
2
iridoviral disease – Jancovich et al. 2005). High densities of alien frogs have resulted in
suppressive effects on native biotic communities and disruption of ecosystem dynamics of
invaded areas (e.g., effects of R. marina to varanid and varanid prey populations in Australia –
Doody et al. 2009). Hybridization of alien frogs with native conspecific and congeneric species
has led to loss of genetically distinct populations or entire species due to genetic swamping (e.g.,
X. laevis in South Africa – Picker 1985). Alien frogs have affected socio-economic activities in
numerous ways, from infrastructure (e.g., localized power outages in Florida, United States,
caused by Cuban tree frog [Osteopilus septentrionalis] – Johnson 2007 as cited in Kraus 2009),
agriculture (e.g., predation of honey bees [Apis mellifera] by R. marina in Australia – Tyler
1994), aquaculture (e.g., predation of fish fry by Chinese bullfrog [Hoplobatrachus rugulosus] in
aquaculture facilities in the Philippines – as Y. Ocampo noted in a Manila Bulletin article on
January 17, 2018), nursery, tourism, and real estate industry (e.g., noise pollution caused by the
coqui frog [Eleutherodactylus coqui] in Hawaii – Kraus et al. 1999, Kraus and Campbell 2002),
and public health (e.g., R. marina as a vector of human pathogens and parasites – Everard 1988;
human fatalities after consumption of R. marina – Rabor 1952).
Diesmos et al. (2006) provided the first review of the status and distribution of alien frogs
in the Philippines that featured five alien frogs namely: the green paddy frog (Hylarana
erythraea [Schlegel 1837]), the cane toad (Rhinella marina [Linnaeus 1758]), the American
bullfrog (Lithobates catesbeianus [Shaw 1802]), the East Asian bullfrog (Hoplobatrachus
rugulosus [Wiegmann 1834]), and the Asiatic painted narrowmouth frog (Kaloula pulchra Gray
1831). Afterwards, a sixth alien frog, the greenhouse frog (Eleutherodactylus planirsotris [Cope
1862]), was reported by Olson et al. (2014). The most recent account of the distribution of these
frogs was provided by Diesmos et al. (2015), but was presented in passing along with
distributions of native Philippine frogs and is still very limited in terms of geographic scope. To
3
date, there remains a huge knowledge gap in the history of alien frog invasions in the
Philippines. Moreover, no recent attempt has been made to synthesize the growing body of
knowledge on their current invasion status and distribution. These knowledge gaps limit our
capacity to adequately assess their risk and ecological and socio-economic impacts. Moreover,
knowledge gaps also limit our capability to develop and implement sound management response
strategies and policies to prevent or mitigate invasions (Wittenberg and Cock 2001, Jeschke and
Strayer 2006, Hulme 2006, 2009, Hulme et al. 2008).
Here, we reconstructed the invasion history and updated the current invasion status and
distribution of the six alien frogs in the Philippines. We focused our study to the historical and
geographical features of their invasion (introduction, establishment, and spread).We approached
this by: (1) assembling a species-distribution database from geographical and historical data; (2)
identifying the origin of propagules, year and locality of first report, and pathways that mediated
their dispersal (introduction) into the Philippines; (3) determining the process of spread, modes
of dispersion, and pathways that mediated their secondary (post-introduction) dispersal
throughout the Philippines; (4) quantifying the rate of spread as revealed by ‘invasion curves’
and ‘proportion curves’; and lastly (5) updating their current invasion status and distribution.
Materials and Methods
Data collection
Geographical data (i.e., species-distribution data) on the six alien frogs in the Philippines
were obtained from several Natural History Collections (NHC) – California Academy of
Sciences (Scheinberg and Fong 2017), Field Museum of Natural History (Grant and Resetar
2017), Florida Museum of Natural History (Blackburn and Brown 2017), Museum of
Comparative Zoology (Harvard University Museum and Morris 2017), National Museum of
Natural History/Smithsonian Institute (Orrell and Hollowell 2017), University of Kansas (Brown
4
2017), University of Texas at Austin (Cannatella and LaDuc 2016), and Spanish National
Museum of Natural Sciences (Spanish National Museum of Natural Sciences [CSIC] 2018),
through the Global Biodiversity Information Facility (GBIF). This was complemented with
historical and geographical data from published and unpublished scientific literature and from
our own field surveys, which were also published online via the GBIF (HerpWatch Pilipinas,
Inc. [HWP] 2019).
Origin and dispersal pathways
The origin and the pathways that facilitated the introduction of the alien frogs were
determined by reviewing scientific literature. In cases where species data on pathways in the
Philippines were lacking, possible pathways were inferred by extrapolating information from
areas where comprehensive documentation is available for the species or from inference based
on the species’ biology and ecology (Essl et al. 2015, Scalera et al. 2016). Pathways were
categorized following the Convention on Biological Diversity’s (CBD) pathways categorization
system (Scalera et al. 2016) – a unified and standardized categorization, hierarchy and
terminology for alien species pathways, which enables consistent and effective prioritization of
pathways and the identification of the best management response (Essl et al. 2015). The CBD’s
system recognizes three broad mechanisms by which alien species may arrive and enter a new
region: importation of commodity, arrival of a transport vector, or spread from a neighboring
region. These mechanisms result to six principal pathways (i.e., pathway categories): intentional
‘release’ in nature, ‘escape’ from confinement, transport-as a ‘contaminant’, transport- as a
‘stowaway’, via a ‘corridor’, and ‘unaided or natural dispersal’. These pathway categories are
further categorized into 44 subcategories (i.e., pathway subcategories) (Scalera et al. 2016; see
document UNEP/CBD/SCSTTA/18/9/Add.1). The CBD’s system, although a generic scheme,
5
was chosen over other developed taxon-specific systems (e.g, the system used by Kraus 2007,
2009 for alien amphibians and reptiles) because it is a broad, internationally-agreed
nomenclature developed for effective science-communication with environmental authorities to
better guide the development and implementation of management strategies and policies against
invasive alien species. A comparison of the CBD’s system and that used by Kraus (2007, 2009)
for alien amphibians and reptiles is shown in supplemental online material Appendix S1.
Spatio-temporal spread and current invasion status and distribution.
To reconstruct the history of the alien frogs’ spread in the Philippines, we partitioned the
assembled species-distribution database into distinct periods based on natural breaks in the
dataset (i.e.,1885 to 1950, 1885 to 1975, 1885 to 2000, 1885 to 2017). Partitions were plotted
separately onto a Philippine map. By examining the spatio-temporal patterns of the alien frogs’
distribution, we identified the potential mechanisms and associated pathways of their secondary
dispersal throughout the Philippines following Wilson et al. (2009) and Scalera et al. (2016),
respectively. Moreover, by examining the alien frogs’ current distribution (Figure 1)
complemented with observations on their invasion (from scientific literature and our own field
surveys), their current invasion status was assessed and categorized following Faulkner et al.
(2016) as modified from Blackburn et al. (2011).
Rate of spread
The rate of spread (i.e., invasion rate) of H. erythraea, R. marina, H. rugulosus, and K.
pulchra was measured using ‘invasion curves’ (sensu Pyšek and Prach 1993). Two species, L.
catesbeianus and E. planirostris, were excluded in this analysis because the former appears to
have failed in establishing breeding populations in the Philippines and we currently have
6
insufficient data for the latter. Because the often unclear site descriptions of records which in
many cases provided only the municipality, province, and/or island as geographic position, it was
not possible to make a GIS-based superimposed grid (e.g., 10 x 10 km square) and use it as a
measure of the rate of spread (Hengeveld 1989). Instead, for each alien species, invasion curves
were constructed using linear-regression models fitted to the log-transformed cumulative number
of first locality records (tested separately under two geographic levels: [1] provincial and [2]
island) plotted against time (starting from year when the species was first record to 2017) and the
slope b of the regression line was used as a proxy of the rate of spread (Pyšek 1991, Pyšek and
Prach 1993). Linear-regressions were modelled using the ‘ggplot2’ R package (Whickham and
Chang 2008) conducted under R platform (R core team 2017). To provide a realistic picture of
the degree of sampling for frogs in the Philippines, we performed the same procedure for native
frogs to construct a “curve of discovery rate,” where the presence of any one of the native frogs
in a locality was enough to consider that locality occupied (i.e., certainly surveyed). Species-
distribution data of native frogs were obtained from the same sources where species-distribution
data of alien frogs were obtained (from NHC complemented with published scientific literature).
The curve of discovery rate represents the degree and spatio-temporal distribution of sampling of
native frogs in the Philippines (Delisle et al. 2003). However, this does not indicate that the
range of native species is expanding over time, but rather their range is simply better known over
time (Delisle et al. 2003). To test the equality of collection rate between alien and native frogs,
the difference between the slope of the regression line of the invasion curve of alien frogs and
that of the curve of discovery rate of native frogs was tested using analysis of covariance
(ANCOVA; Chambers and Hastie 1992) using the ‘stats’ R package conducted under R platform
(R core team 2017). In principle, the more abrupt the slope of the invasion curve, the more
rapidly the alien frog has spread (Pyšek and Prach 1993). It is noteworthy, however, that the
7
slope may have been affected by the temporal changes in the degree of sampling, where an
abrupt slope may indicate high degree of sampling during a limited time period (Delisle et al.
2003). Nonetheless, the slope only estimates the rate of spread and cannot be used to distinguish
periods of different levels of expansion (Delisle et al. 2003).
Use of data from different sources suffers from several biases, of which spatio-temporal
variation in sampling effort is the most concerning. These biases may drastically affect the
quality of reconstructed invasion histories, potentially resulting to misleading interpretations and
applications (Graham et al. 2004, Estoup and Guillemaud 2010, Newbold 2010, Lavoie 2013).
Here, we accounted for variation in spatio-temporal sampling effort by using a simple and
reliable method for objectively delineating periods of expansion of alien species – ‘proportion
curves’ (Delisle et al. 2003). For each alien frog, the proportion curve was constructed by, first,
dividing the cumulative number of first locality records of the alien frog by the cumulative
number of first locality records of the pooled native frogs; then, plotting obtained proportions
against time (Delisle et al. 2003). Increasing proportions (of alien frog vs. native frogs) for a
particular time period suggests that the invasive range (in the Philippines) of the alien frog is
indeed expanding, because it is expanding faster than if it was strictly the result of better spatial
coverage of sampling effort. A phase of expansion was defined as a time period of at least 5
years during which the proportion is increasing more than 5%. Stable proportions (i.e., new
specimens of alien frog and native frogs were collected at the same time) suggest that the
invasive range of the alien species may still be expanding, but this could simply be related to
better spatial coverage of sampling effort focused on alien frogs. Declining proportions (negative
slopes on the proportion curve) don’t necessarily indicate declining alien frog populations, but
instead may be due to the invasive range of the alien frog expanding at a very slow rate (i.e.,
additional localities occupied by the alien frog are rarely found) (Delisle et al. 2003). Declining
8
proportions may also mean that the founder populations of the alien frog may be growing within
a certain locality (i.e., province, island), but no new first records in other localities were
documented (Mosena et al. 2018).
Results
Invasion history of alien frogs in the Philippines
Green paddy frog (Hylarana erythraea [Schlegel 1837])
Hylarana erythraea (Family Ranidae) is native to South Asia, mainland Southeast Asia
(Myanmar, Thailand, Lao People’s Democratic Republic, Cambodia, Viet Nam, and Peninsular
Malaysia), Borneo, and some Islands of Indonesia (Sumatra, Java, Lombok, and Riau Islands). It
has been introduced in the Philippines and Sulawesi Island (Indonesia) (Diesmos et al. 2006,
Frost 2016). Overlooked in earlier studies, a specimen that was collected on “Isla de Samar”
(Samar Island in central Philippines) in 1885 (CSIC 2018) is the earliest confirmed record of the
species in the Philippines. Subsequently, it was found on neighboring islands of Negros,
Sibuyan, and Tablas (also central Philippines) (Taylor 1920, Taylor 1922, Inger 1954). It was
initially thought to be native to the Philippines until Inger (1954) proposed it to be classified as
an alien species based on the observed unnaturally disjunct distribution of the then known
Philippine populations, exclusively found in central Philippines (Figure 1) with the nearest extra-
Philippine populations on Borneo (located southwest of the Philippines) . It is speculated to have
been introduced as a contaminant of agricultural commodities (i.e., ‘food contaminant’ – Scalera
et al., 2016) imported from Borneo Island by Sulu seafarers (Inger 1954).
In the initial years of its invasion, H. erythraea was known only from the central
Philippines, and was reported on Luzon Island in the north and Mindanao Island in the south
9
(two largest Philippine islands) only in the late 1990s. It spread throughout the Philippines by a
combination of leading-edge dispersal and long-distance dispersal (‘cultivation’, a mechanism of
dispersal wherein propagules are actively moved and receive resources to establish/persist –
Wilson et al. 2009). It may have secondarily dispersed at long-distances through three plausible
pathways: (1) as a contaminant of locally-transported agricultural commodities (i.e., food
contaminant) as was the case of its introduction and the recent range expansion of co-occurring
native frog species (e.g., Asiatic tree frog [Polypedates leucomystax], Philippine oriental frog
[Occidozyga laevis], and Philippine grass frog [Fejervarya vittigera] – Inger 1954, Brown and
Alcala 1970a, Brown et al. 2010); (2) as a contaminant of locally-transported or traded food fish
fingerlings (i.e., contaminant on animals) owing to its propensity to occur in water bodies where
fish fingerlings are often collected; and (3) as escapees of gardens since it is sold as an attractive
addition to garden ponds (i.e., ornamental purpose other than horticulture) along with terrestrial
and aquatic ornamental plants (Sy 2014) (Table 1).
At the provincial level, the slope of the regression line of the invasion curve of H.
erythraea (b = 0.12) and that of the curve of discovery rate (b = 0.13) does not differ
significantly (P = 0.27) (Figure 2a). Meanwhile, at the island level, the slope of the regression
line of the invasion curve of H. erythraea (b = 0.0108) is slightly less steep than that of the curve
of discovery rate (b = 0.0134) and is significantly different (P < 0.001) (Figure 2c). Proportion
curves showed three major periods of expansion at the provincial level: 1908–1922, 1961–1970,
and 1989–2006 (Figure 2b); and three major periods of expansion at the island level: 1908–1923,
1948–1962, and 1993–1997 (Figure 2d).
Hylarana erythraea is now a fully invasive species (i.e., “E” invasion status; individuals
dispersing, surviving, and reproducing at multiple sites across a greater or lesser spectrum of
habitats and extent of occurrence – Blackburn et al. 2011) and was recorded to have been present
10
so far in 39 provinces (out of 81) on 20 major islands (Table 2, Figure 1). It is highly tolerant of
human disturbance, occurring in exceptional numbers in artificial aquatic habitats, such as rice
fields and garden ponds, as well as natural aquatic habitats near human habitation, such as
swamps, ponds, ditches, creeks, and rivers (Alcala 1955, Alcala 1986, Alcala and Brown 1998,
Gaulke 2011). It was also reported to be present in riverine habitats of secondary forest at low-
and mid-elevations (Alcala 1955, Brown and Alcala 1961, Brown and Alcala 1970b, Siler et al.
2012) and has penetrated primary-growth forests (Diesmos et al. 2006, Brown 2017, Scheinberg
and Fong 2017).
<<Table 1 near here>>
<<Table 2 near here>>
<<Figure 1 near here>>
<<Figure 2 near here>>
Cane toad (Rhinella marina [Linnaeus 1758])
Rhinella marina (Family Bufonidae) is native to tropical America. It has been released in
the wild as a biological control in many parts of the world, including several countries in Africa,
South America (outside its native range), Asia, and Oceania (including Pacific Islands) (Esteal
1981, Kraus 2009, Frost 2016). Similarly, it was released in the Philippines as a biological
control for insect and rodent pest in agricultural fields (Merino 1936, Rabor 1952, Soriano 1964).
Initially, 28 toads were acquired from the Hawaiian Sugar Planters Association and were brought
to the Philippines in 1934 (Merino 1936). Toads were first reared on Luzon Island, initially at the
Bureau of Plant Industry compound, Manila, and later in the College of Agriculture of the
University of the Philippines – Los Baños, Laguna Province (Rabor 1952).
11
From 1934–1949, R. marina was dispersed by human-mediated long-distance dispersal
(cultivation) in six provinces on five major islands as a biological control (Figure 1) (Rabor
1952, Soriano 1964). From sites of initial release, it spread intra-island via ‘leading-edge
dispersal’, as was observed by Rabor (1952) on Negros Island. It is noteworthy that most of the
records for human-mediated spread were lost during the liberation of Manila during World War
II (Rabor 1952). When deemed ineffective in curbing crop pests in the 1950s, it dispersed long-
distances (‘mass dispersal’, a mechanism of dispersion where a dispersal route is established –
Wilson et al. 2009) throughout the Philippines (Figure 2) as a hitchhiker on ships/boats (rather
than being dispersed as a biological control), having been observed by one of us (A.C.D.) on a
ship plying the route from Batangas province (Luzon Island) to Busuanga Island of Palawan
province. It may have also dispersed long-distances as a stowaway in container/bulk having been
transported through such means and subsequently intercepted from entering uninvaded
Australian states (Henderson and Bomford 2011) and New Zealand (Chapple et al. 2016).
Moreover, ‘corridors’ (a physical connection of suitable habitat linking a portion of a range to
another area – Wilson et al. 2009; e.g., tunnels and bridges) likely facilitated its dispersion
between islands separated by biogeographic barriers; for example, the San Juanico Bridge
provides a corridor which connects the islands of Samar and Leyte (Table 2).
At the provincial and island level, the slope of the regression line of the invasion curve of
R. marina (b = 0.0154 and 0.0167, respectively) is steeper than that of the curve of discovery
rate (b = 0.0109 and 0.0167, respectively), but does not differ significantly (P = 0.012 and 0.06,
respectively) (Figure 2a,c). Several major periods of expansion can be distinguished in its
proportion curves: at the provincial level, 1944–1951, 1961–1970, and 1999–2006 (Figure 2b);
and at the island level, 1945–1954, 1983–2017 (Figure 2d).
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Rhinella marina is now a widespread invasive and is the most widespread among the six
alien frogs, having been observed so far in 54 provinces on almost all major islands (36 islands)
in the Philippines except for the islands of the Provinces of Batanes (northernmost group of
islands of the Philippines) and Palawan (westernmost group of islands of the Philippines) (Table
2, Figure 1). Whenever encountered, R. marina occurs in abundant numbers, usually in the
vicinity of human habitation, in artificial habitats, such as agricultural, cultivation, and
agroforestry areas, and in mixed and disturbed aquatic and terrestrial habitats, such as forest
edges and secondary-growth forests (Rabor 1952, Alcala 1986, Alcala and Brown 1998, Gaulke
2011). It has also been seldom observed in pristine primary-growth forests (Denzer et al. 1994,
Delima et al. 2007), along coastal areas, mangroves, tidal gravel beaches, tidal water bodies,
cavesm(Denzer et al. 1994, Belleza and Nuñeza 2014), and in high-elevation habitats, such as the
mountain summits of Mount Makiling (1090 meters above sea level) and Mount Arayat (1026
masl) (Diesmos 1998).
American bullfrog (Lithobates catesbeianus [Shaw 1802])
Lithobates catesbeianus (Family Ranidae) is native to Eastern North America (Frost
2016). It was introduced in many parts of the world, including several countries in Africa,
Central and South America, Asia, and Europe, primarily for hunting in the wild (Kraus 2009). In
the Philippines, twenty four mature individuals were imported from Louisiana, United States, in
1966 by a private entrepreneur for captive propagation (Pascual 1987a). In the 1960s, soon after
successful acclimatization, the first bullfrog-breeding center was established on Luzon Island in
Barangay San Rafael, Montalban and Barrio Kambal, San Mateo, Rizal Province (Ugale 1976,
Pascual 1987b,c) (Figure 3). Subsequently, in 1976, the Philippine Bullfrog Industry, Inc. (PBII),
a private-owned, for-profit corporation, was established and supplied the high foreign demand
13
(primarily from the United States) of bullfrog specimens for biomolecular and medical research
(Pascual 1987a, Urbanes 1988, Urbanes 1990, Matienzo 1990).
Through the National Bullfrog Development Project (NBDP), a five-year program
orchestrated by the Ministry of Natural Resources (now the Department of Environment and
Natural Resources) and in cooperation with PBII, another seven bullfrog breeding centers were
established across the Philippines from 1980–1985 (Natural Resources Development
Corporation of the Ministry of Natural Resources [NRDC-MNR] 1981, Buenviaje 1983,
Inovejas 1985). The NBDP was a government effort to develop the bullfrog industry, which
promoted the production of breeders for distribution to prospective raisers to develop both local
and foreign markets (Buenviaje 1983, Inovejas 1985). Bullfrog breeding centers housed
thousands of individuals in different life stages and were established on Luzon Island (Mt.
Arayat National Park, Pampanga Province; Paoay, Ilocos Norte Province), Mindanao Island
(Cotabato City, Cotabato Province; Nabunturan, Davao del Norte Province [now Compostela
Valley Province]; Tacurong, Sultan Kudarat Province), Mindoro Island (Socorro, Oriental
Mindoro Province), Leyte Island (Babtangon, Leyte Province), and Panay Island (Tangalan,
Aklan Province) (NRDC-MNR 1981, Buenviaje 1983, Inovejas 1985) (Table 2, Figure 3, see
supplemental online material Appendix S2). Most, if not all, bullfrog breeding centers ceased
operation soon after the termination of the NBDP in 1985 (NRDC-MNR 1987).
<<Figure 3 near here>>
During the operation of bullfrog breeding centers and farms in the Philippines from the
1970s to 1980s, numerous individuals of L. catesbeianus frequently escaped from confinement
by their own means or aided by natural calamities, such as extensive floods (Diesmos et al. 2006,
T. Padamada, former Pond Foreman of the Bullfrog Breeding Production Center in Paoay, Ilocos
Norte, pers. comm.). Moreover, on Luzon Island (Paoay Lake and some areas in Batac, Ilocos
14
Norte Province) and Mindanao Island (Lagusan Marsh, Cotabato Province, Maguindanao
Province), government programs promoted the release in the wild of thousands of individuals for
hunting (Inovejas 1985). Similarly, individuals were released in environs of bullfrog breeding
centers after the termination of the NBDP (T. Padamada, pers. comm.).
To date, the status of L. catesbeianus in the Philippines – whether it has successfully
established in the wild or failed– is undetermined (i.e., introduced/casual; ‘B3’ invasion status;
Individuals transported beyond limits of native range, directly released into a novel environment,
and fate unknown or may be extinct from novel environment – Blackburn et al. 2011, Faulkner et
al. 2016) (Table 2). Recently, a sighting was reported on Luzon Island (Paoay Lake and Biloca,
Ilocos Norte Province), but we failed to confirm this in recent surveys in the same area. Previous
reports of this species could be misidentified H. rugulosus.
East Asian bullfrog (Hoplobatrachus rugulosus [Wiegmann 1834])
Hoplobatrachus rugulosus (Family Dicroglossidae) is native to East Asia (China and
Taiwan) and Mainland Southeast Asia (Myanmar, Thailand, Lao People’s Democratic Republic,
Cambodia, Viet Nam, and Peninsular Malaysia). It has been introduced to Borneo and the
Philippines (Alcala et al. 1995, Inger and Tan 1996, Frost 2016). It was first reported in the
Philippines in 1993 on Luzon Island (University of the Philippines – Los Baños, Laguna
Province) (Figure 2) (Alcala et al. 1995, Alcala and Brown 1998, Diesmos 1998, Diesmos et al.
2006). In the same year, it was also reported in other areas on Luzon Island (Metropolitan
Manila), Mindanao Island (Davao del Sur Province), Mindoro Island (Occidental Mindoro
Province and Oriental Mindoro Province), and Panay Island (Iloilo Province) (Figure 1)
(Diesmos et al. 2006).
15
Diesmos et al. (2006) hypothesized that H. rugulosus was farmed alongside L.
catesbeianus through the NBDP in 1980s. However, its farming was not mentioned in any of the
reports of NBDP (NRDC-MNR 1981, 1987). It was likely introduced to the Philippines in the
1990s (post-NBDP) through four pathways: (1) escaped by own means from bullfrog farms (i.e.,
farmed animals); (2) released for hunting in the wild as was the case of its introduction on
Borneo (Inger 1996, Inger and Stuebing 1997); (3) as a contaminant with other transported
animals (i.e., imported live fish fingerlings) as was the case of the introduction of its congener,
the Indian bullfrog Hoplobatrachus tigerinus, in Andaman Island, India (Mohanty and Measey
2018); or (4) stowaway in transported container/bulk in as much as individuals were intercepted
from entering New Zealand through such means (Chapple et al. 2016). The exact origin of
introduced individuals is unknown. From areas of first report, H. rugulosus dispersed throughout
the Philippines by leading-edge dispersal and by long-distance dispersal (cultivation and mass
dispersal) (Table 1). The same pathways inferred to have facilitated its introduction may have
also facilitated its secondary dispersal throughout the Philippines (Table 1).
At the provincial level, the slope of the regression line of the invasion curve of H.
rugulosus (b = 0.0308) is steeper than that of the curve of discovery rate (b = 0.0177) and differs
significantly (P < 0.001) (Figure 2a). Meanwhile, at the island level, the slope of the regression
line of its invasion curve (b = 0.0106) is less steep than that of the curve of discovery rate (b =
0.0259) and is significantly different (P < 0.0001) (Figure 2c). Proportion curves showed two
major periods of expansion at province level: 1998–2005 and 2012–2014 (Figure 2b) and an
apparent major period of invasiveness from 1998–2001 at the island level (Figure 2d).
Hoplobatrachus rugulosus is now a fully invasive species and has been reported so far in
27 provinces on seven major islands (Table 2, Figure 1). It is most abundant in disturbed low
elevation aquatic habitats, such as rice fields, ponds, lakes, and rivers (Alcala et al. 1995,
16
Diesmos et al. 2006, Gaulke 2011). Breeding populations were observed in aquatic habitats in
pristine, old-growth forests (Diesmos et al. 2006, Brown 2017).
Asiatic painted narrowmouth frog (Kaloula pulchra Gray 1831)
Kaloula pulchra (Family Microhylidae) is native to Southern East Asia (China), Eastern
South Asia (Bangladesh and India), Mainland and Maritime Southeast Asia (Myanmar, Thailand,
Lao People’s Democratic Republic, Cambodia, Viet Nam, Peninsular Malaysia, Singapore, and
some islands of Indonesia [ Sulawesi]). It has been introduced in Borneo, Guam, Taiwan, and the
Philippines (Inger and Steubing 1997, Diesmos et al. 2006, Christy et al. 2007a,b, Kuangyang et
al. 2016, Frost 2016). It was first reported in the Philippines in 2003 from three localities on
Luzon island (Metropolitan Manila, Laguna Province, and Bulacan Province) (Figure 1)
(Diesmos et al. 2006).
It was initially thought that K. pulchra escaped from the exotic pet trade (i.e.,
pet/aquarium/terrarium species) (Diesmos et al. 2006). However, the fact that it is of negligible
interest in the Philippine exotic pet trade and that sold individuals were locally collected suggests
that the pet trade is an unlikely pathway for its introduction into the Philippines (Sy 2014). It
may have been introduced into the Philippines through three pathway subcategories: contaminant
of nursery materials (Diesmos and Brown 2011, Sy 2014); hitchhikers on ship/boat since
individuals were observed onboard a ship from Borneo (Inger 1966); and stowaways in
transported container/bulk since individuals have been intercepted from entering Australia
(Henderson and Bomford 2011), Guam (Christy et al. 2007b), and New Zealand (Chapple et al.
2012) through such means. The exact origin of introduced individuals is unknown, but they may
have come from Borneo. Its spatio-temporal pattern of distribution shows that it spread by
leading-edge dispersal and long-distance dispersal via cultivation and mass dispersal (although
17
corridors via tunnels and land-bridges is also a possible mechanism of dispersal) (Table 1). The
same pathways that facilitated its introduction into the Philippines could have also facilitated its
secondary dispersal throughout the country (Table 1).
At the provincial level, the slope of the regression line of the invasion curve of K.
pulchra (b = 0.0575) is almost equal to that of the curve of discovery rate (b = 0.0577) and does
not differ significantly (P = 0.9581) (Figure 2a). Meanwhile, at the island level, the slope of the
invasion curve (b = 0.0692) is steeper than that of curve of discovery rate (b = 0.042 and is
significantly different (P < 0.001) (Figure 2c). Proportion curves show an apparent major period
of invasiveness at the provincial level from 2004–2015 (Figure 2b).
Since the first report, K. pulchra has spread in all directions throughout the Philippines,
reported so far in 16 provinces on six major islands, and is now a fully invasive species (Table 2,
Figure 1). It occurs in abundant numbers in the vicinity of human habitation and artificial and
natural terrestrial and aquatic habitats, such as agricultural, cultivation, and agroforestry areas,
forest edges, and secondary-growth forests (Siler et al. 2011, McLeod et al. 2011, Bucol et al.
2011, Brown et al. 2012b, Brown et al. 2013, Brown 2017).
Greenhouse Frog Eleutherodactylus planirostris (Cope 1862)
Eleutherodactylus planirostris (Family Eleutherodactylidae) is native to Cuba and the
Bahamas. It has been introduced to several countries in North America, Central America, Africa,
Guam (USA), Hawaii (USA), the Philippines, Hong Kong (China), and Singapore (Hedges et al.
2004, Olson et al. 2014, Olson 2016, Frost 2016). It was first reported in the Philippines in
Davao City, Davao del Sur Province, Mindanao Island, in 2014, but is believed to have been
introduced in the late 2000s (Olson et al. 2014). It was introduced into the Philippines as a
contaminant of imported or re-exported ornamental plants or nursery materials (i.e., contaminant
18
nursery materials) that may have originated from Hawaii. This pathway is also reported for its
introduction to Hawaii (Kraus et al. 1999). Moreover, it most likely dispersed long-distances
(cultivation) throughout the Philippines through the same introduction pathway.
Eleutherodactylus planirostris is now a fully invasive species recorded so far in eight
provinces on seven major islands (Table 3, Figure 2). Established populations have been
observed in disturbed terrestrial habitats, such as gardens and immediate vicinities of human
habitation (Olson et al. 2014, Sy et al. 2015).
Discussion
By gathering and analyzing geographic and historical data on the invasion of alien frogs
in the Philippines, we present a comprehensive documentation of their history of invasion and
updated their current invasion status and distribution. We showed that six alien frogs have been
introduced in the Philippines since the 1880s, chronologically: H. erythraea, R. marina, L.
catesbeianus, H. rugulosus, K. pulchra, and E. planirostris. Four pathway categories (falling in 8
subcategories) facilitated their introduction: intentional ‘release’ for biological control and
hunting in the wild; ‘escape’ from farms; ‘contamination’ of agricultural commodities, fish
stocks, and nursery materials; and ‘stowaway’ on container/bulk and (hitchhiker on) ship/boat.
Spatio-temporal patterns of distribution (Figure 2) showed that alien frogs dispersed through
two main mechanisms: ‘leading-edge dispersal’ and long-distance dispersal primarily via ‘mass
dispersal’ and ‘cultivation’ (‘corridors’ also facilitated the spread of some alien frogs between
islands connected by man-made land bridges such as the San Juanico Bridge that connects the
islands of Samar and Leyte) (Table 1). The pathways that mediated their secondary dispersal
were either the same as those of their introduction or included or shifted to other pathways over
time (Table 1). For H. erythraea, R. marina, H. rugulosus, and K. pulchra, the slope of invasion
19
curves varied between species and between geographic levels, wherein K. pulchra is spreading
fastest (Figure 1). Similarly, their proportion curves showed several periods of expansion at the
geographic levels of province and island (Figure 1). Five alien frogs (H. erythraea, R. marina,
H. rugulosus, K. pulchra, and E. planirostris) are now fully invasive species, whereas L.
catesbeianus has been released in the wild for hunting, but it is unclear if the species has
successfully established viable populations (Table 2, Diesmos et al. 2006). Among the
widespread invasive frogs, R. marina is the most widespread while E. planirostris is the least
distributed (Figure 1, Table 2). We further discuss here implications of our findings and provide
recommendations for invasive alien-frogs management in the Philippines.
Introduction pathways
Our findings show temporal variation in the importance of different pathways that
facilitated the introduction of the alien frogs in the Philippines (Table 1). Contamination of
transported commodities (i.e., transport-contaminant) and stowaways on transporting vessels and
associated equipment and media (i.e., transport-stowaway) are the most important and current
pathways for alien frog introductions, having facilitated the introduction of the two most recent
introduced alien frogs (K. pulchra and E. planirostris in the 2000s). The importance of this
pathway in alien frog introductions has also been observed in several island and island
archipelagoes such as Guam (Christy et al. 2007a,b), Hawaii (Kraus et al. 1999), and Singapore
(Ng and Yeo 2012), as well as in other parts of the world (Kraus 2009, Capinha et al. 2017).
Meanwhile, the last documented intentional release of an alien frog was in 1990s. This pattern
has been similarly observed in global alien amphibian and reptile species introductions (Kraus
2009), and in other alien-vertebrate species introductions in island archipelagoes such as
Galapagos Islands (Phillips et al. 2012) and continental areas such as Europe (Hulme et al. 2008)
20
and South Africa (Faulkner et al. 2016). Interestingly, recent studies on interceptions of alien
species in Australia (Henderson and Bomford 2011) and New Zealand (Chapple et al. 2016)
suggested that substantially more amphibian and reptile species are being moved via transport-
stowaway than previously thought, owing to the lack of comprehensive biosecurity measures in
other jurisdictions (Chapple et al. 2016).
Changes in pathway of introduction and long-distance dispersal
Our findings show that the pathways that facilitated the introduction and secondary
dispersal of alien frogs in the Philippines may vary, and that pathways that facilitated secondary
dispersal may have changed over time. For instance, so far, the introduction and secondary
dispersal of L. catesbeianus, K. pulchra, H. rugulosus, and E. planirostris are most likely
through the same pathways. In contrast, in the initial years of its invasion, R. marina was
introduced in the Philippines as biological control and was similarly dispersed by humans to
several islands throughout the archipelago through the same pathway. The importance of this
pathway decreased and was soon deemed insignificant by the 1950s when R. marina’s ability to
curb the population of crop pests was found to have been ineffective and when studies abroad
that demonstrated the ecological impacts of R. marina’s invasion deterred its use as a biological
control agent (Rabor 1952, Eastael 1981, Diesmos et al. 2006). It has since dispersed at long-
distances by hitchhiking on boats/ships, as was observed by A. C. Diesmos on a ship plying
Batangas Province, Luzon Island, to Busuanga Island, Palawan Province. Further, It has often
been intercepted as a stowaway in container/bulk in New Zealand (Chapple et al. 2016),
suggesting the possibility of that it may utilize this pathway to disperse throughout the
Philippines. Another example is the case of H. erythraea, which was introduced as a contaminant
of agricultural commodities and was similarly secondarily dispersed at long-distances through
21
the same pathway. Moreover, given that it is sold for ornamental purpose other than horticulture
(Sy 2014), it may have been transported to different islands for commercial purposes and,
subsequently, escaped from garden ponds. Further, its propensity to live in aquatic habitats
where fish fingerlings are usually extracted for translocation suggests that its contamination of
translocated fish fingerlings (i.e., contaminant on animals) may have as well facilitated its long-
distance dispersal, as was the case of F. moodiei (previously identified as F. cancrivora), a co-
occurring Philippine native species, that has been introduced to Guam (Christy 2007a).
Spatio-temporal pattern of spread and associated pathways
Spatio-temporal patterns of distribution showed that the spread of alien frogs throughout
the Philippines followed a stratified diffusion process, which involves an initial range expansion
through leading-edge dispersal (i.e., neighborhood diffusion) and new colonies (i.e., foci) that are
successively created through human-mediated long-distance dispersal events (Van der Plank
1967, Hengeveld 1989, Shigesada et al. 1995, Higgins and Richardson 1999). For invading
organisms, especially species that associate closely with humans, a stratified diffusion process of
spread “seems to be the rule rather than the exception” (Higgins and Richardson 1999) (e.g.,
Argentine ants Linepithema humile in the United States [Suarez et al. 2001], red fire ants
Solenopsis invicta in United States [Porter et al. 1988], and the common ragweed Ambrosia
artemisiifolia in France [Chauvel et al. 2006]). Given the innate limitations in amphibians’
natural dispersal capabilities, it can be said that the inter-island spread of the alien frogs
throughout the Philippines is primarily by long-distance dispersal via cultivation and mass
dispersal, and facilitated by several pathways (Table 1). Meanwhile, the intra-island spread of
alien frogs is predominantly through unaided leading-edge dispersal and, especially for larger
22
islands such as Luzon and Mindanao, long-distance dispersal which was likely facilitated by
same pathways that facilitated inter-island long-distance dispersal (Table 1).
Current invasion status and distribution
We presented here an updated, comprehensive, and detailed account on the invasion
status and current distribution of all known alien amphibian species in the Philippines (Table 2,
Figure 1). A significant body of data from previously overlooked published and unpublished
literature, natural history collections from several museums, as well as our personal observations
were included for the first time. We reported evidence that H. erythraea, R. marina, H.
rugulosus, K. pulchra, and E. planirostris are now fully invasive species, having established
populations in the wild, with individuals dispersing, surviving, and reproducing at multiple sites,
typically the dominant species in both artificial and disturbed habitats, and are continuously
spreading throughout the Philippines (Blackburn et al. 2011, Faulkner et al. 2016). Meanwhile,
the status of L. catesbeianus in the Philippines is undetermined. We identified the localities
where breeding centers of L. catesbeianus were established in the 1960s to 1980s, as well as
release sites (Figure 3, see supplemental online material Appendix S2). Until further surveys are
conducted in these areas, we remain cautious in determining the status of L. catesbeianus in the
Philippines. It is noteworthy that recent field surveys conducted by the authors in Northern
Luzon Island (Paoay, Ilocos Norte Province – one of the sites where bullfrog breeding centers
were formerly established) failed to report the occurrence of L. catesbeianus.
We showed that R. marina is currently the most widely-distributed alien frog, having
dispersed to almost all Philippine islands, except on the islands in the provinces of Palawan
(westernmost Philippines) and Batanes (Northernmost Philippines) (Figure 1). However, the fact
that individuals of R. marina were observed by A.C. Diesmos hitchhiking on a ship from
23
Batangas Province, Luzon Island, to Busuanga Island, the northernmost island of Palawan
Province, in 1995, emphasizes the need for surveys on Busuanga Island. Meanwhile, it is also
possible that R. marina has already been introduced to islands of Batanes Province, due to the
availability of potential pathways – hitchhikers on ships/boats. The availability of such pathway
is supported by the recent dispersal of a Philippine native species, Polypedates leucomystax,
possibly as a contaminant of agricultural commodities, onto Batanes Island of Batanes Province
(Brown et al. 2010). It is noteworthy that R. marina has already reached Tawi-Tawi Island,
Tawi-Tawi Province, which is its current southernmost range in the Philippines and is about 50
km from Borneo.
There have not been significant changes in the distribution of H. erythraea and H.
rugulosus since the review of Diesmos et al. (2006), with only a few new provincial and island
records (Figure 1). Meanwhile, the distribution of K. pulchra in 2006 was restricted to three
provinces on Luzon Island. Since then, it has rapidly dispersed across 16 provinces on six islands
(Figure 1). Lastly, this is the first review on the status and distribution of E. planirostris in the
Philippines (Figure 1). Established populations of E. planirostris have only been observed in
artificial habitats, and it is anticipated to disperse into natural habitats in the future, as in the case
in Hawaii (Olson et al. 2012).
Rate of spread and projected distribution in the future
Our findings show that H. erythraea, R. marina, H. rugulosus, and K. pulchra are
continuously spreading, wherein K. pulchra is spreading fastest. Invasion curves show that the
alien frogs, especially for the cases of the most widespread – H. erythraea and R. marina – have
not reached spatial saturation, suggesting that the species will continue to spread (Figure 2).
Meanwhile, proportion curves (Figure 2) showed that the alien frogs seem to have undergone
24
several periods of expansion during the course of their invasion in the Philippines. Such periods
of expansion may reflect coincidental increase in human transportation and commerce or
temporal and species sampling bias owing to the increased interest in Philippine frogs and
invasive alien species during the past 30 years (Diesmos et al. 2006, Diesmos et al. 2014).
Management recommendations for alien frog invasions in the Philippines
Our findings provide much needed-science based information that can help guide the
development and implementation of sound management strategies for current and future alien
frog invasions in the Philippines. Local trends (as presented in this study) as well as global trends
(Kraus 2009) on alien frog introductions show that transport-contaminant and transport-
stowaway pathways are highly likely to mediate future alien frog introductions in the country
and, thus, should be a priority for management and legislation. Further, the future importance of
these introduction pathways is manifested in the trend in the Philippines’ international trade,
travel, and transport; the magnitude of arriving imported commodities (an annual average of
about 404.6 million kilos of agricultural commodities, 370 thousand kilos of live fish, and 1.5
million kilos of nursery materials from 2011–2015) and sea traffic (an annual average of about
10 thousand foreign ship calls, 1.6 million 20-foot unit containers, and 62.4 million metric tons
of cargo from 2011–2015) (Philippine Ports Authority 2015, Philippine Statistical Authority
2016) can be said to present high propagule pressure and, hence, risk of future alien species
introduction through these pathways. Although none of the alien frogs in the Philippines was
introduced through ‘escape from confinement’ pathway as pet/aquarium/terrarium species, the
fact that this pathway is currently a major introduction pathway for global vertebrate species
(Hulme et al. 2008), including frogs (Kraus 2009), and that the local undocumented pet trade of
alien frogs is notoriously rampant in the Philippines (Sy 2015), emphasizes the need to improve
25
or develop stricter regulations for the local pet trade. Finally, despite the recent decreasing
importance of the ‘release in nature’ pathway in global and Philippine alien frog introductions,
management strategies and legislation are needed to prevent future introductions through this
pathway.
We elucidated here the current distributions of the alien frogs, through point-locality
maps complemented with species-distribution database (HWP 2019), which can help guide
decision-making and the strategic spatial implementation of management schemes (Stohlgren
and Schnase 2006, Stohlgren and Jarnevich 2009). For instance, the maps show that K. pulchra
and H. rugulosus are only known from a few islands; their spread to other islands should be
controlled or prevented. Having also demonstrated in this study the paramount importance of
human-mediated long-distance dispersal in the spread of alien frogs in the Philippines, we
recommend focusing on preventing their secondary long-distance dispersion onto novel areas
(i.e., uninvaded islands) through pathway-specific approaches, rather than focusing efforts on
leading-edges of invasions (Moody and Mack 1988). This should also integrate schemes to
eliminate new incursions through frequent surveys of susceptible sites (e.g., ports-of-entry,
nurseries and garden centers, etc.) and rapid eradication of incursions (Moody and Mack 1988).
Acknowledgements
We thank the Ministry for the Environment of the Government of Japan through the
ecological monitoring data mobilization grant (BIFA3_26) of Global Biodiversity Information
Facility (GBIF) –Biodiversity Information Fund for Asia (BIFA), the Philippine Department of
Environment and Natural Resources (DENR) through their Foreign-Assisted Special Projects,
and the Biodiversity Management Bureau (BMB) of the DENR through GEF-UNEP Removing
Barriers to Invasive Species Management in Production and Protection Forests in Southeast Asia
26
(FORIS) Project. ANP thanks the Science Education Institute (SEI) of the Philippine Department
of Science and Technology (DOST) through the Accelerated Science and Technology Human
Resource Development Program (ASTHRDP) for the M.Sc. Scholarship and National
Geographic Science and Exploration Asia Young Explorers grant (ASIA 57-16). ANP thank Dr.
John Measey for reviewing and providing critical points of improvement on an earlier version of
the manuscript, and for finding time to provide his most expert advice on invasion biology. Prof.
Richard Thomas B. Pavia, Jr., Prof. Carmela P. Española, and Prof. Jonathan A. Anticamara
suggested improvements to the M.Sc. thesis version of this manuscript. We thank Ms. Lara Jane
Mendoza for editing the English of the manuscript. We extend our sincerest thanks to the
institutions that gave us access to their holdings and information facilities: the Philippine
Department of Agriculture, Science Education Institute of the Philippine Department of Science
and Technology, and Ecosystems Research and Development Bureau of the Philippine
Department of Environment and Natural Resources, and all local and international Natural
History Collections with herpetological collections from the Philippines.
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Tables
Table 1. Introduction pathways, mechanism(s) of secondary (post-introduction) dispersal, and associated secondary dispersal pathways of the
alien frogs in the Philippines.
Introduction Dispersal
Introduction pathway category
Introduction pathway sub-category
Mehanism(s) ofdispersal
Secondary dispersal pathway category
Secondary dispersal pathway sub-category
Hylarana erythraea Transport-contaminant Food contaminant Cultivation Transport-contaminant Food contaminant
Contaminant on animals
Escape from confinement Ornamental purpose other than horticulture
Leading-edge Unaided Natural dispersal
Rhinella marina
Release in nature Biological control Cultivation Release in nature Biological control
Mass dispersal Transport-stowaway Container/bulk Hitchhikers on ship/boat
Leading-edge Unaided Natural dispersal
Corridor Corridors Tunnels and land bridgesLithobates catesbeianus
Release in nature Hunting in the wild Cultivation Release in nature Hunting in the wild
Escape from confinement Farmed animals Escape from confinement Farmed animals
Hoplobatrachus rugulosus
Release in nature Hunting in the wild Cultivation Release in nature Hunting
Escape from confinement Farmed animals Escape from confinement Farmed animals
Transport-contaminant Contaminant on animals Transport-contaminant Contaminant on animals
Transport-stowaway Container/bulk Mass dispersal Transport-stowaway Container/bulk
42
Leading-edge Unaided Natural dispersalKaloula pulchra
Transport-contaminant Contaminant nursery material Cultivation Transport-contaminant Contaminant nursery material
Transport-stowaway Container/bulk Mass dispersal Transport-stowaway Container/bulk
Hitchhikers on ship/boat Hitchhikers on ship/boat Leading-edge Unaided Natural dispersal
Corridor Corridors Tunnels and land bridgesEleutherodactylus planirostris
Transport-contaminant Contaminant nursery material Cultivation Transport-contaminant Contaminant nursery material
Pathway and pathway sub-categories were classified following Scalera et al. (2016). Mode of dispersal was classified following Wilson et al. (2009).
43
Species OriginLocality/Localities first
recorded
Periodintroduce
d
Distribution in thePhilippines
Invasion status in thePhilippines6
Islandspresen
t
Provincespresent
Invasion
category
Invasionstatus
Hylarana erythraea Unknown Samar Island 1800s1 20 39 E Widespread invasive
Rhinella marina Hawaii,UnitedStates
Metropolitan Manila andLaguna Province, Luzon
Island
19342 36 54 E Widespread invasive
Lithobates catesbeianus Louisiana,UnitedStates
Rizal Province, LuzonIsland
19663 5 12 B3 Casual/Introduced
Hoplobatrachus rugulosus Unknown Laguna Province andMetropolitan Manila,Luzon Island; Iloilo
Province, Panay Island;Occidental Mindoro and
Oriental MindotoProvince, Mindoro Island
1990s4 7 27 E Widespread invasive
Kaloula pulchra Unknown Metropolitan Manila,Laguna Province, and
Bulacan Province, LuzonIsland
2000s4 6 17 E Widespread invasive
Eleutherodactylus planirostris
Hawaii,UnitedStates
Davao del Sur Province,Mindanao Island
2010s5 7 8 E Widespread invasive
Table 2. Origin, first geographic records, and current invasion status and distribution of the six alien anuran species in the Philippines.
1CSIC (2018); 2Merino (1936); 3Pascual (1987a); 4Diesmos et al. (2006); 5Olson et al. (2014); 6Invasion category and invasion status of the alien amphibians in the Philippines were classified following Faulkner et al. (2016) as modified from Blackburn et al. (2011). Invasion category E defined are fully invasive species, with individuals dispersing, surviving and reproducing at multiple sites across a greater or lesser spectrum of habitats and extent of occurrence; Invasion category B3 defined as individuals transported beyond limits of native range, and directly released into a novel environment (fate unknown).
44
Figure 1. Point-locality maps of the Philippine invaded-range distribution of (from left toright) Hylarana erythraea, Rhinella marina, Hoplobatrachus rugulosus, Kaloula pulchra, andEleutherodactylus planirostris through time. Species distribution records (black dots) werepartitioned into periods: before 1950, before 1975, before 2000, and after 2000-Presentandplotted onto Philippine map. The year and location of first species record(s) is/areindicated.
45
.Figure 2. Rate of spread of (from left to right) Hylarana erythraea, Rhinella marina,Hoplobatrachus rugulosus, and Kaloula pulchra. The invasion curve of each alien frog (solidlines and closed circles) was compared with the curve of discovery rate of native frogs takenas a whole (dotted lines and open circles) at province (A) and island (C) level. Results areexpressed as the logarithm of the cumulative number of new provincial or island records overtime. Invasion rate (slope b of the regression equation) is given for each alien frog and for thenative frogs as a whole. The difference (P value) between the slope of linear regressionmodels of alien frogs and that of native frogs as a whole is given for each alien frog.Proportion curves (logarithm of the cumulative number of new provincial or island recordsfor alien species divided by that for native species taken as a whole) at province (B) andisland (D) level was calculated for each year on record for the four alien frogs. Periods ofexpansion, as determined by a positive slope extending for at least five years, are indicated bygrey zones.
46
Figure 3. Point locality map of the established bullfrog breeding centers and farms in the
Philippines from 1960s to 1980s.
47
Supplemental Materials
Appendix S1. Comparison of pathway categorization system of the Convention on
Biological Diversity (Faulkner et al. 2016) and Kraus (2007, 2009).
CBD category pathway
CBD sub-category pathwayKraus 2007, 2009 category pathway
Release in nature
Biological control Biocontrol
Hunting in the wild Food
Introduction for conservation purposes Conservation
Release in nature for use (other than above, e.g., fur, transport, medical use)
Medicine
Landscape/flora/fauna “improvement” in the wild
“intentional”
Other intentional release “intentional”, religious, lab release
Erosion control/ dune stabilization
Fishery in the wild (including game fishing)
Escape from confinement
Pet/aquarium/terrarium species (including live food for such species)
Pet trade
Ornamental purpose other than horticulture
Botanical garden/zoo/aquaria (excluding domestic aquaria)
Zoo trade*, exhibit
Farmed animals (including animals left under limited control)
Food
Research and ex-situ breeding (in facilities) Research
Live food and live bait Duck food, bait use
Agriculture (including Biofuel feedstock)
Aquaculture / mariculture
Forestry (including reforestation)
Fur farms
Horticulture
Transport-contaminant
Food contaminant (including of live food) Cargo stowaway
Timber trade Cargo stowaway
Contaminant nursery material Nursery trade
Contaminant on animals (except parasites, species transported by host/vector)
Aquaculture contaminant
Parasites on animals (including species transported by host and vector)
Contaminant on plants (except parasites, species transported by host/vector)
48
Parasites on plants (including species transported by host and vector)
Seed contaminant
Contaminated bait
Transportation of habitat material (soil, vegetation, …)
Transport-stowaway
Container/bulk Cargo stowaway
Machinery/equipment Cargo stowaway
People and their luggage/equipment (in particular tourism)
Cargo stowaway
Hitchhikers in or on airplane Aircraft stowaway
Hitchhikers on ship/boat (excluding ballast water and hull fouling)
Boat
Ship/boat ballast water Ballast
Vehicles (car, train, …) Vehicle
Other means of transport
Angling/fishing equipment
Organic packaging material, in particular woodpackaging
Ship/boat hull fouling
CorridorInterconnected waterways/basins/seas
Tunnels and land bridges
UnaidedNatural dispersal across borders of invasive alien species that have been introduced through pathways 1 to 5.
Spread from adjacent introduction
*CBD pathway subcategories in grey and italicized is unlikely to or have not to date been reported to facilitate the dispersal of an alien frog.
49
Appendix S2. Location of bullfrog breeding centers and bullfrog farms in the Philippines where the American bullfrog (Lithobates
catesbeianus) was bred from 1960s to 1980s.
Species Longitude Latitude Island Province Municipality Yaer Source Remarks
Lithobates catesbeianus 121.2508 14.7744 Luzon Island Rizal Montalban 1966 Ugale 1976 Bullfrog farm
Lithobates catesbeianus 121.1333 14.6667 Luzon Island Rizal San Mateo 1966Buenviaje 1983, Inovejas 1985, Pascual 1987, Ugale 1976 Bullfrog farm
Lithobates catesbeianus no data no data Luzon Island Rizal no data 1970s Matienzo 1990 Bullfrog farm
Lithobates catesbeianus no data no data Luzon Island Laguna no data 1970s Matienzo 1990 Bullfrog farm
Lithobates catesbeianus no data no data Luzon Island Bulacan no data 1970s Matienzo 1990 Bullfrog farm
Lithobates catesbeianus no data no data Luzon Island Bataan no data 1970s Matienzo 1990 Bullfrog farm
Lithobates catesbeianus 120.5371 18.1205 Luzon Island Ilocos Norte Paoay 1980s Buenviaje 1983, Inovejas 1985 Bullfrog breeding center
Lithobates catesbeianus 120.7167 15.2 Luzon Island Pampanga Magalang 1980s Buenviaje 1983, Inovejas 1985 Bullfrog breeding center
Lithobates catesbeianus 121.4 13.05 Mindoro Island Oriental Mindoro Soccoro 1980s Buenviaje 1983, Inovejas 1985 Bullfrog breeding center
Lithobates catesbeianus 122.25 11.7667 Panay Island Aklan Tangalan 1980s Buenviaje 1983, Inovejas 1985 Bullfrog breeding center
Lithobates catesbeianus 124.85 11.4167 Leyte Island Leyte Babatngon 1980s Buenviaje 1983, Inovejas 1985 Bullfrog breeding center
Lithobates catesbeianus 125.9667 7.6 Mindanao Island Compostela Valley Nabuntaran 1980s Buenviaje 1983, Inovejas 1985 Bullfrog breeding center
Lithobates catesbeianus 124.2312 7.2015 Mindanao Island Maguindanao Cotabato City 1980s Buenviaje 1983, Inovejas 1985 Bullfrog breeding center
Lithobates catesbeianus 124.2833 6.5833 Mindanao Island Maguindanao Liguasan Marsh 1980s Diesmos et al. 2006 Release sites
Lithobates catesbeianus 124.679 6.7015 Mindanao Island Sultan Kudarat Tacurong City 1980s Buenviaje 1983 Bullfrog breeding center
Lithobates catesbeianus no data no data Mindanao Island Maguindanao no data 1980s Buenviaje 1983 Release sites
Lithobates catesbeianus 120.5 18.0667 Luzon Island Ilocos Norte Batac City 2002 Diesmos et al. 2006Reported sightings (unverified)
Lithobates catesbeianus 120.579 18.2 Luzon Island Ilocos Norte Batac City 2002 Diesmos et al. 2006Reported sightings (unverified)
Lithobates catesbeianus 120.5333 18.1 Luzon Island Ilocos Norte Laoag 2002 Diesmos et al. 2006Reported sightings (unverified)
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