INVASION BIOLOGYCOURSE MANUAL

INVASION BIOLOGY COURSE MANUAL

UNEP-GEF Project (0515): Removing Barriers to Invasive Species Management in Production and Protection Forests in Southeast Asia (FORIS Project)

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DISCLAIMER This activity was conducted as part of UNEP/GEF Project No. 0515 Removing Barriers to Invasive Species Management in Production & Protection Forests in Southeast Asia (FORIS Project). UNEP is the Project Implementing Agency whereas CABI is the Executing Agency; The Project National Implementing Agency in the Philippines is the Department of Environment & Natural Resources through the Biodiversity Management Bureau. The presentation of material in this document and the geographical designations employed do not imply the expression of any opinion whatsoever on the part of any of the agencies involved, concerning the legal status of any country, territory, or area, or concerning the delimitation of its frontiers of boundaries.

PREFERRED WAY TO CITE THIS PUBLICATION Department of Environment and Natural Resources-Biodiversity Management Bureau (DENR-BMB). (2016). Course Manual on Invasion Biology. Quezon City: Department of Environment Biodiversity Management Bureau and Natural Resources. pp. i-iv, 1-60. Cover photos (clockwise): rice black bug Scotinophara coarctata (Normandy Barbecho), coronitas Lantana camara (Danilo Tandang), rice field rate Rattus exulans (Maria Josefa Veluz), Chinese softshell turtle Pelodiscus sinensis (Emerson Sy), variable squirrel Callosciurus finlaysonii (Pola Geneva Bumanglag), African tulip Spathodea campanulata (Danilo Tandang).

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TABLE OF CONTENTS

ABOUT THIS COURSE .............................................................................................................................. 1

UNIT 1: INTRODUCTION TO INVASION BIOLOGY ................................................................................... 2

1. 1 OVERVIEW OF THE COURSE ................................................................................................... 2

1. 2 INVASIVE SPECIES TERMINOLOGY .......................................................................................... 5

1. 3 CHARACTERISTICS AND ATTRIBUTES OF INVASIVE ALIEN SPECIES ...................................... 10

UNIT 2: PATHWAYS TO INVASION ........................................................................................................ 17

2. 1 THE INVASION PROCESS ....................................................................................................... 17

2.2. UNDERSTANDING AND PREDICTING INVASIONS ................................................................. 26

UNIT 3: IMPACT AND MANAGEMENT OF IAS ....................................................................................... 36

3. 1 IMPACTS OF INVASIVE ALIEN SPECIES .................................................................................. 36

3. 2 MANAGEMENT OF INVASIVE ALIEN SPECIES........................................................................ 41

3. 3 GLOBAL AND NATIONAL POLICIES ........................................................................................ 50

APPENDICES .......................................................................................................................................... 53

LIST OF FIGURES

Figure 1. A simplified definition of invasive alien species (IAS) ............................................................. 3

Figure 3. Clarias macrocephalus, maximum size 120 cm. Illustration from Rainboth, W.J. 1996 ......... 4

Figure 2. Clarias gariepinus maximum size 170 cm. Photo by Kin Loon taken in Shah Alam, Selangor,

Malaysia (FishBase) ................................................................................................................ 4

Figure 4. Golden Apple Snail Pomacea caniculata, Photo taken from www.knowledgebank.irri.org .. 4

Figure 5. The Invasion Process of IAS (Adapted from Casal, 2006) ...................................................... 18

Figure 6. Arachis sp. in bloom, utilized for forage as well as an ornamental plant. ............................ 20

Figure 7. Micropterus salmoides (Lacepède, 1802) caused the disappearance of some local fishes in

Lake Caliraya. Illustration from Eccles 1992......................................................................... 21

Figure 8. The janitor fish Pterygoplichthys pardalis (Castelnau, 1855) caught in Laguna. Photo by

Rodolfo Reyes, Jr. ................................................................................................................. 21

Figure 9. Rhinella marina, an old invasive species in the Philippines. Photo by Arvin C. Diesmos. ..... 23

Figure 10. Ballast water in ships, loading and discharging containing several species from WWF

publication. Silent invaders.

https://upload.wikimedia.org/wikipedia/commons/2/2a/Ballast_water_en.svg .............. 24

Figure 11. P. managuensis (Gunther, 1867) is now present in several Philippine waterbodies. Photo

by R. B. Reyes, Jr. .................................................................................................................. 24

Figure 12. Water hyacinth Eichhornia crassipes. Photo by Danilo N. Tandang .................................... 29

Figure 13. Mozambique tilapia Oreochromis mossambicus. Figure from Rainboth, 1996. ................. 30

Figure 14. Impacts of IAS ...................................................................................................................... 36

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Figure 15. Knifefish Chitala ornata in Laguna de Bay. Photo by Cripsina Muan/ Laguna Lake

Development Authority ....................................................................................................... 38

Figure 16. Janitor fish Pterygoplichthys disjunctivus. Photo by Don T. Dumale .................................. 38

Figure 17. The golden apple snail Pomacea canaliculata in a rice paddy. Photo by Ravindra Joshi. .. 39

Figure 18. Ipil-ipil Leucaena leucocephala. Photo by Danilo N. Tandang. ........................................... 39

Figure 19. Paper mulberry Broussonetia papyrifera female (left) and male (right). Photo by Danilo N.

Tandang. .............................................................................................................................. 40

Figure 20. Holistic management of IAS ................................................................................................ 44

LIST OF TABLES Table 1. Boundaries between Classical Biology and Invasion Biology .................................................. 5

Table 2. Definition of Terms (modified from Falk-Petersen, 2006) ....................................................... 5

Table 3. Pathways of Invasion of IAS in the Philippines ....................................................................... 25

Table 4. Potential Management Strategies for Invasive Alien Plant Species ....................................... 44

Table 5: Potential Management Strategies for Invasive Alien Animals ............................................... 45

Table 6. Principles of Good Ecological Restoration Practice ................................................................ 48

Table 7: Attributes of Accessing Restoration Programs ...................................................................... 49

LIST OF BOXES Box 1: Introduction of Game Species in the Philippines ...................................................................... 22

Box 2: Examples of Invasive Alien Species ........................................................................................... 29

Box 3: Observed and Projected Climate Changes ................................................................................ 31

Box 4: Climate Change and IAS Affect Biodiversity .............................................................................. 32

Box 5: Ecosystem Services ................................................................................................................... 37

Box 6: Example of an IAS Management Strategy - The Pams Approach ............................................. 46

Box 7. Example of an IAS Management Strategy - Ecological Restoration .......................................... 47

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ABOUT THIS COURSE

Welcome to Invasion Biology: the Study of Invasive Alien Species, an introductory course under the Bachelor of Science degree in Biology, Environmental Science, Agriculture, and other related fields. In this course we will be discussing basic information that every Filipino citizen needs to know about Invasive Alien Species. The course will provide students with information on:

What invasive alien species are, characteristics of successful invasive alien species

Why were they introduced, intentional and unintentional introductions, vectors of introduction and subsequent spread

Impacts (ecological, economic, sociological, health and recreational consequences);

Some examples of invasive alien species in the Philippines

Invasive species in the context of global climate change – double trouble

Invasive species management: prevention, EDRR, control and restoration eradication

The first unit will focus on introducing what these species are, while the 2nd unit will focus on the invasion process and explain how the species have moved beyond their natural boundaries. The 3rd unit will focus on the impacts and management of invasive species.

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UNIT 1: INTRODUCTION TO INVASION BIOLOGY

Unit 1: Introduction to Invasion Biology 1.1 Overview of the course 1.2 Invasive species terminology 1.3 Characteristics and Attributes of Invasive Species

At the end of Unit 1, you should be able to:

Understand why we need to know about invasive alien species

Understand the difference between an alien species and an invasive alien species

Be familiar with some terminologies used in invasion biology; and

Identify characteristics/traits or attributes of an invasive alien species

1. 1 OVERVIEW OF THE COURSE

Alien or exotic species are brought to the Philippines for a wide variety of reasons (e.g. ornamental, agriculture, aquaculture, etc.). Some of the alien species are pre-adapted to the environmental conditions of the Philippines and have been able to establish, reproduce and proliferate to the detriment of biodiversity, crop and pasture production, human and animal health, water resources, etc. are called invasive alien species (IAS). Still others although they have survived, reproduced have not been reported as having adverse impacts, they remain to be called alien species. We get back to them later in this course. The introduction of new species into the Philippines has contributed to the Filipino diet and way of life. Fruits, flowers, vegetables, fish, pets and a lot more species that we take for granted are actually introduced or alien. The Convention on Biological Diversity CBD defines alien species as ‘a species, subspecies or lower taxon, introduced, includes any part, gametes, seeds, eggs, or propagules of such species that might survive and subsequently reproduce outside its natural past or present distribution.’ The lychees or litseyas (Litchi chinensis Sonner, 1782) (Family: Sapindaceae) is a species which has been introduced or brought to the Philippines. It was not present in the country prior to its introduction. It is an alien species – alien to the Philippines. The plant, seedlings, branches or seeds may survive, grow and bear fruit – all are equally known as alien species. Subspecies or varieties of this plant are also called alien species. The International Council for the Exploration of the Sea (ICES) defines an introduced species as ‘any species accidentally or intentionally transported and released by humans into an area outside its present range (1994, 1999). Invasive alien species (IAS) on the other hand are ‘alien species whose introduction and/or spread threaten biodiversity (CBD). The International Union for the Conservation of Nature (IUCN) defines IAS as ‘an alien species which become established in natural or semi-natural ecosystems or habitat, are agents of change, and threaten native biological diversity.’ (https://www.cbd.int/invasive/terms.shtml) Some alien species have brought socioeconomic benefits to specific sectors of society; however some have become invasive and may have harmful effects on biodiversity and natural resources.

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Figure 1. A simplified definition of invasive alien species (IAS)

IAS can also affect human life and health and cause serious economic damage to agriculture, forestry and fisheries. IAS are one of the most important direct drivers of biodiversity loss and modifications in ecosystem service (EU, 2014). However, most Filipinos are not aware of them. Although we talk about new types of food available in the market (new fruits, fishes, vegetables, etc.), new diseases of plants animals and humans, species that before were only seen in pet shops but are now found in lakes, forests or even gardens, we do not correlate these with IAS. IAS are not given much attention and they are not flagged. IAS pose the greatest threat to fragile ecosystems such as islands (Veitch et al., 2011), as exemplified by the archipelagic nature of the Philippines. Islands are special ecosystems that have allowed the evolution of new species because of their geographic isolation, hence endemism is high in island ecosystems like the Philippines. Endemic species are species which are found only in a particular area and nowhere else. Philippine endemic species are species which are found only in the Philippines. The loss of an endemic species is not just a loss to Philippine biodiversity but to global biodiversity as well. Since species loss or extinction is not reversible, any threat to endemic or native species survival should not be taken lightly. Several species have been introduced into the Philippines by well-meaning agencies, organizations and individuals. However these introductions sometimes failed to take into consideration the fact that these are living entities capable of reproducing and spreading to areas where it was not introduced and will be eating to survive, occupying a niche (vacant or previously occupied) and so on. So easily, it may become a competitor for food and niche of the native species or a predator of an existing species. For instance, the African catfish (hito) (Clarias gariepinus (Burchell 1822) (Family: Clariidae)) was introduced into the country for food (Froese and Pauly, 2016). It has contributed to the variety of food available to us as another protein source. However, it has outcompeted our native catfish (Clarias macrocephalus Günther, 1864 (Family: Clariidae)) for the niche and food. Most of the catfish caught and sold in the market have been identified as the new species (African catfish), while the native catfish is seldom encountered in markets today. This means that the African hito is now more common

Alien species

Establish (survive and reproduce)

Stay localized

No impact Impact

Invasive Alien Species

Spread

No impact Impact

Invasive Alien Species

Does not establish

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or abundant than our native hito. Figure 2 shows the African catfish, which grows up to 170 cm, while our native catfish grows up to 120 cm (Figure 3). Clearly, the wide disparity in the sizes of the catfishes may point to the reason why the African catfish was introduced.

Another example is the golden apple snail (Family Ampullariidae) (Pomacea caniculata (Lamarck 1822) and Pomacea maculata (Perry 1810)). The golden apple snail was brought to the Philippines as an addition to the Filipino diet and as a possible export commodity. It grew faster than our native kuhol (Pila luzonica (Reeve 1856) and thus it was raised for possible export abroad. This species however was so successful that it was able to escape from aquaculture confinements and invade other ecosystems like rice fields (Figure 4). When the species reached the rice fields, they ate the young tillers, thus reducing rice tillers which in turn significantly reduced yield. In 1990, costs associated to snail infestation alone in the Philippines were estimated to be between USD425-1,200 million (Naylor,

1996). This excludes human health and environmental issues. Other than this, the golden apple snails out-competed the native kuhol, drastically reducing the population of the native species. The ultimate irony is that the golden apple snail was not preferred by Filipinos as food substitute to the native kuhol. The native kuhol was now beset by a double population stress whammy – competition by the golden apple snails and continuous harvesting for the delicacy. The examples provided are only some of the invasive alien species which have been introduced into the Philippines. More species have been introduced and have become invasive.

Raising awareness on the issue and providing up‑to‑date scientific information is an essential requirement to combating IAS. This course aims to raise awareness on one of the major causes of species extinctions so that future introductions of potential invasive alien species are avoided.

Figure 3. Clarias gariepinus maximum size 170 cm. Photo by Kin Loon taken in Shah Alam, Selangor, Malaysia (FishBase)

Figure 4. Golden Apple Snail Pomacea caniculata, Photo taken from www.knowledgebank.irri.org

Figure 2. Clarias macrocephalus, maximum size 120 cm. Illustration from Rainboth, W.J. 1996

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1. 2 INVASIVE SPECIES TERMINOLOGY The field of invasion biology is an expansion beyond ‘classical biology’. Classical biology is concerned with organisms within their natural distribution. Invasion biology deals with traits of introduced alien (non-native) species, their ability to spread, interactions with each other and with native species in new ecosystems (Falk-Petersen, 2006). Table 1 shows an adaptation of a figure from Falk-Petersen, 2006 defining the boundaries of classical and invasion biology. Table 1. Boundaries between Classical Biology and Invasion Biology

NATIVE INTRODUCTION NON-NATIVE

Natural distribution

Nat

ura

l bo

un

dar

y

Spread by human vectors New/Receiving ecosystems

Natural migration Air transport, land transport and water transport

Naturalization

Invasion

Domain of “Classical Biology” Domain of Invasion Biology

Like any other developing field of science, several terminologies have been utilized to describe alien species and invasive alien species. Below is a table on terms utilized in literature on invasion biology. Table 2. Definition of Terms (modified from Falk-Petersen, 2006)

Term Definition

Native/indigenous An organism occurring within its natural past or present range and dispersal potential (organisms whose dispersal is independent of human intervention)a

Endemic Organism restricted to a specified region or locality

STUDY ACTIVITIES/QUESTIONS 1.1

Species introductions have changed some of our ecosystems. From the short write up in Section

1-1, 1. What is the difference between alien and invasive alien species?

1. List down at least 5 species in the Philippines that are: a. alien but not invasive and b. alien and invasive

2. Where are they found in the Philippines?

Example: 1. Species: Broussonetia papyrifera (paper mulberry) 2. Philippine distribution: The species has been found in several areas in the Philippines

and has taken over huge patches of land in widespread in Butuan City about 60 kms from the city going to Davao City.

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Term Definition

Non-native/ alien/

adventive/ exotic/

foreign/ introduced/ non-

indigenous/ novel

An organism occurring outside its natural past or present range and dispersal potential including any parts of the organism that might survive and subsequently reproduce (organisms whose dispersal is caused by human action)a

Introduction Direct or indirect movement by humans, of an organism from its native past or present range to a range outside its distribution potential (natural distribution)

Transfer/ translocation/

transplantation

Human mediated movement of an organism within its past or present range and dispersal potentialb

Escape Non-native organism, or part of organism that might survive and subsequently reproduce, originally domesticated, now found in the wildc

Feral Native organism, or part of organism that might survive and subsequently reproduce, originally domesticated but now reverted to its original wild stated

Transient/ casual Native or non-native organisms that may occur and reproduce occasionally in an area, but do not form self-replacing populations and rely on repeated introductions for their persistence.

Established Native or non-native organism that has obtained a self-sustaining population in an area it previously did not occur

Naturalized A non-native organism that has obtained a self-sustaining population

Reintroduced Organism intentionally released into a part of former range from which it had become extirpated or extincte

Re-established Re-colonization and establishment of an organism in a part of former range from which it had become extirpated or extinct

Re-stocking Release of an organism into an area in which it is already present to supplement the population

Invasive Alien organisms that have established in a new area and are expanding their range and have negative impact to other species or to the ecosystemf

Pest Organisms considered harmful to human activitiesg

Weed Plants growing in areas where they are not wanted

Environmental weeds Non-native plant taxa invading natural vegetation affecting native biodiversity and/ or ecosystem functioning

Transformers Organisms that change the character, condition, form or nature of a natural ecosystem over a substantial areah

Physical ecosystem

engineer

Organisms that directly or indirectly control the availability of resources to other organisms by causing physical state changes in abiotic or biotic materialsi

a Modified from IUCN 2000; b Modified from ICES 1995, FAO 1996 and IUCN 1995; c Modified from Godman and Payne 1996, IUCN 2000; d Modified from Morris 1992 and Bullock et al. 1997; e Modified from WWF 1976, IUCN 1987, IUCN 1995 and Bullock et al. 1997; f Modified from Binggeli 1994 and Mack 2000; g Modified from Morris 1992; h Wells et al. 1986; i Jones et al. 1997

Native/indigenous – the terms native and indigenous have been utilized in varied contexts. It may refer to the organism’s distribution in relation to its attached dispersal ability or its presence in an environment within a defined time period. Natural communities – are dynamic and continuously expand or retract their spatial distribution (for example some plants have a wider distributional range during rainy seasons but during dry seasons

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they are not found in the area). It is difficult to distinguish native species (existing in an area due to their own means of dispersal – seeds brought by tides from Island A to Island B and growing and reproducing there) from those which have been introduced through human interventions (e.g. seeds brought by a migrant from Island A to Island B and also growing and reproducing there or other species brought in via ballast water of ships). On the other hand, utilizing specific temporal criteria is also problematic as there is often a lack of data on the actual historical status of a particular species as well as they could include human-aided dispersal of organisms prior to the proposed dates. When you talk to old people sometimes they can provide information on what species were there and what were not present during their youth. This may provide you with information on whether a species is new to the area or not. However, we have to remember that a species may have been introduced over 100 years ago. So, even if they have been there for a long time, they are still introduced, e.g. species which have been brought to the Philippines during the Spanish era or earlier? Humans are the force which drives species beyond their natural dispersal limitation, their actions allowed species to be present beyond their natural distribution. Even if we are not sure whether the species is native or introduced, the meaning of the terms denoting naturally occurring species is clear. Native species are those whose distribution is independent of humans. Endemic – is a more restricted term, denoting a species which occurs only in a restricted region. The geographic scale of ‘restricted area’ obviously influences the degree to which an endemic species differs from a native species. A species may be endemic to a particular ecosystem, region, country or continent. For example, when one says that a species is only found in a specific lake, and nowhere else, we say that the species is endemic to that lake. If a species is only found in a particular region in the Philippines, we say that the species in endemic to that region in the Philippines (it may be present in several lakes in the region but never found outside the region) and so on. The thing to remember here is exclusivity. A species found exclusively in an area is endemic to that area. Non-native/alien/adventive/exotic/foreign/introduced/non-indigenous/novel – the terms include the absence of the organism prior to a certain time period, and that its presence is human-mediated. It has some impact in the new area and that the species has established self-reproducing populations. The terms also refer to a species, subspecies, or lower taxon, introduced outside its natural past or present distribution. This includes any part, gametes, seeds, eggs, or propagules of such species that might survive and subsequently reproduce (CBD COP6 Decision VI/23, 2002). Simply put, all of those terms have the same meaning: these are species whose distribution has been a result of human-mediated activities. Oreochomis mossambicus (Peters, 1852) (Family: Cichlidae) (one of the species called tilapia) has been moved around the world for aquaculture. O. mossambicus, a freshwater African species would not have naturally dispersed to as far as Asia or the Americas on its own. They have been brought to these continents by humans. Tilapia is non-native to Asia and the Americas. Introduced species – refers to species directly or indirectly brought by humans from its native past or present range to a range outside its distribution potential (natural distribution). It does not connote establishment. Most species introduced into a new ecosystem does not necessarily establish self-reproducing populations (Williamson, 1996). A tropical species introduced to the arctic for example would have a hard time adapting to its new environment. Introduced species refers to the transfer of species by humans, either indirectly or directly, of an alien species outside its natural range (past or present); this transfer can be either within a country or between countries or areas beyond national jurisdiction (COP 6). Using the tilapia as an example, tilapia which is native to Africa has been introduced to the Philippines and over 100 other countries around the world (Froese and Pauly, 2016).

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Transferred/translocated/transplanted – these terms are being used to describe human mediated movement of species within their native range as opposed to the introduced species which are used for species being moved beyond their natural range and dispersal potential. A simple illustration of this term is for example, Species A is present in two areas (Areas 1 and 2), however, Species A in Area 1 has already dwindled in population size, humans may transfer/translocate/transplant some individuals of Species A in Area 2 to Area 1. Escaped/feral (for domesticated species) – these terms refer to introduced domesticated plants and animals that are found in the wild and have reverted to their wild state. An example is an ornamental fish that have lost its ‘domesticated traits’ such as its specific color breed. A Poecilia reticulata Peters, 1859 (Family: Poeciliidae) in an aquaria have a very different color from the individuals in the wild, sometimes enhanced by feeds, so when the specific feed is modified from the aquaria to the wild, the coloration of the specimen changes. Transient/casual – introduced species which have not formed ‘self-sustaining’ populations; they are only present in the new environment up to their lifespan. One may say that these are species which, although they are pre-adapted to or survived in the local environment, were not able to reproduce hence as they age and die, the species are lost. Naturalized/established – Introduced species that have self-sustaining populations. A naturalized species need not become invasive. The CBD defines naturalized or established species as alien species in a new habitat, which have successfully produced viable offspring with the likelihood of continued survival (CBD COP6). Some introduced fruit trees have been called naturalized/established. The avocado has been introduced to the Philippines and has become established. Reintroduced – introduction of organisms into a part of former natural range from where it has been extirpated. Reintroduction is often done to conserve species. Species A population has been lost in Area 1, however, a few towns away (Area 2) a population of Species A has been discovered. Conservationists may bring some individuals from Area 2 and re-introduce them to Area 1 in order to have Species A in Area 1 again. Re-establishment – refers to the action by which the species itself manages to recolonize a former area. If the reintroduction of Species A in Area 1 becomes successful, that is it manages to survive, reproduce and maintain a self-sustaining population, then we say that Species A has re-established in Area 1 likes wolves in parts of Europe. Re-stocking – cover releases of organisms to supplement wild populations already present. The government is currently restocking Laguna de Bay of Oreochromis niloticus as part of their seeding program. This means that they regularly stock the lake with tilapia fingerlings to supplement the feral population of tilapia in the lake even though the species have a self-sustaining population. Some countries restock their waterbodies of native species to add to the wild population for their recreational activities (e.g. fishing). Invasion – Invasion refers to both indigenous and non-indigenous species that spreads, with the aid of humans, in natural or semi natural habitats, producing a significant change in composition, structure, or ecosystem processes or causing severe economic losses to human activities (Copp et al., 2005). Invasive – refer to non-native organisms that expand their range of their own accord but have negative connotation, or lead to an environmental problem. Invasive alien species have been touted to be a major cause of species extinction, second only to habitat extinction. We will be discussing this in great detail throughout this semester.

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Pest/weed – A pest or a weed has a negative effect on humans or are perceived as unwanted in terms of economy, health or environment. It can be both native and non-native. You see them in your gardens, houses, and almost everywhere. Transformers – organisms that change the character, condition, form or nature of ecosystems over a substantial area relative to the extent of that ecosystem. Some plants have allelopathic properties which restricts the growth of other organisms. Overgrown plants sometimes stifle specific areas and allow only certain species to thrive changing the utility of an ecosystem. Physical system engineers – organisms controlling the availability of resources to other organisms. A prime example is the water hyacinth – which blocks the entry of oxygen and light into overrun waterbodies making it impossible for other species to survive. Traffic is terrible in Metro Manila for a long time, peaking at certain times of the day when people start going to work and then again when people go home after work. A ferry service has been initiated to relieve some of the traffic along Guadalupe to Plaza Mexico in Intramuros. This has proved to be a less stressful commute, however, there are times of the year when the water hyacinth have a surge of growth and have become traffic obstructions. The ferries have to slow down to evade the thick water hyacinth vegetation as they wrap around propellers of ferries damaging them. In some areas, water hyacinth have covered the breadth of waterways. Environmental weeds – non-native plants affecting biodiversity and/or ecosystem functioning. Examples of environmental weeds are numerous; these may include ornamental tree species (whose seeds may have been brought by bird droppings or have hitchhiked on animals) which have encroached over areas of native grasslands, blocking light needed by the native species to grow. Environmental weeds are considered invasive, if moved to a new area from an area where they are already non-native then they are invasive. Animal populations dependent on these small shrubs are thus compromised. Lockwood et al., 2007 has also provided an exhaustive list which includes: adventive, alien, casual, colonizing, cryptogenic, escaped, established, exotic, foreign, immigrant, imported, introduced, invasive, naturalized, non-indigenous, noxious, nuisance, pest, ruderal, tramp, transformer, transient, translocated, transplanted, transported, waif and weed. The inconsistency of usage has created a problem with regards to synthesis and management of the invasive alien species. The important thing to remember here is that there are natural and human-mediated rapid range expansion. When we talk about invasive alien species, we are talking about species that have been introduced outside their native distributional range with human mediation.

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1. 3 CHARACTERISTICS AND ATTRIBUTES OF INVASIVE ALIEN SPECIES There are a lot of introduced or alien species in the Philippines. Some have remained confined in areas where they have been brought to. Others, on the other hand, have become invasive. They have successfully colonized the areas where they have been introduced and have gone beyond the initial areas. The invasive alien species (IAS) have survived, reproduced and spread or dispersed in their new environments. In this section, we will learn about the biological characteristics that make some species invasive.

A. Characteristics of Invasive Alien Species (IAS)

a. Survival in the new environment - A species arriving in a new environment must survive before it can even reproduce. There are a lot of things involved in species survival: climate suitability, food and niche availability. Characteristics which may allow them to do so would include:

a. 1. Phenotypic plasticity - Maybe a simple word to describe this is adaptability. The species should be able to tolerate new environmental conditions. This means that it would have a wide environmental envelope. Environmental envelopes are environmental tolerances of species. A species with a wider environmental envelope can thrive in a wider range of environmental conditions. Here we talk of the species being able to survive wider temperature ranges (a species from a temperate environment when introduced into a tropical environment can still survive), moisture ranges, dryness ranges, salinity ranges, long or short solar exposure, etc. Oftentimes, they have a wider distribution range. It is widely adapted to a variety of conditions and would thrive on the available niches within the new environment.

a. 2. Generalists - A generalist species is able to make use of a variety of different

resources (for example, a heterotroph with a varied diet). A specialist species can only

STUDY ACTIVITIES/QUESTIONS 1-2:

1.2.1. From the 10 species you have initially selected in SAQ 1-1, what terminologies have been

used for them? 1.2.2. Make a simple table of your selected species identifying which are alien species and which

are invasive alien species with columns denoting alien and invasive alien species. Use the knowledge you have gained in placing them in the right column. You may want to check the internet for species information.

Sample:

Species Alien but not reported as

invasive

Invasive Alien Species

Why did you place them in the column?

Species A Yes No It is not native to the Philippines and there has been no impact reported for this species to date.

Species B Yes Yes It is not native to the Philippines but there has been adverse environmental impact reported for this species.

Species C No No This is a native species.

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thrive in a narrow range of environmental conditions or has a limited diet. An opportunistic feeder would always have something to eat in the new environment to ensure their survival. It may be able to survive on most food types.

a. 3. Grows and matures in a short period - Species which grow and mature fast

are more likely to increase its population size in a shorter amount of time. This is true for both terrestrial and aquatic species, in most if not all taxa. A plant which flowers and bears fruits at a young age is more likely to have several generations in a given time span. Sometimes species that produce smaller seeds are also less likely to survive. Fishes which grow fast and mature in a short time would also double in number in fewer years.

a. 4. Long-lived - Long-lived species are more likely to be in the new environment

for a longer time, enough time so that they could be able to seek for niches, find mates, seek for new types of food to include in their diet and just generally adapt to the new environment. Species longevity matter.

a. 5. Maximum size - This is a tricky characteristic. Some species may have been

chosen for introduction because of their size (they grow larger than the native species) and were nurtured until they have escaped confinement and became invasive, like the African catfish. However, a lot of ornamental fishes are quite small (also grow fast and mature early) and they have become invasive as well like the mosquito fish. It is the same with plants, there are small and large invasive species, from weeds to some ornamental plants.

b. Reproduction potential - After surviving the new environment, the next hurdle for the

species to be continuously present in the environment is to be able to reproduce. Other set of characteristics are now involved for this. Some species rely on a single species for pollination while others may have several species acting as their pollinators. Species with specific pollinators are dependent on the specific species for its seed production and hence survival. The loss or decrease in the population of the specific pollinator is thus directly correlated to the survival of the plant.

Species with several types of pollinators will allow these plants to have higher chances of being pollinated thereby producing more seeds. This bodes well for the species survival rate. In the same manner, species which dispersed by more than one way is more likely to survive and be spread than those which are being dispersed by a specific way.

b. 1. Method of reproduction - The type of reproduction of known IAS is not

limited to those reproducing sexually or asexually. Species reproducing sexually or asexually may become invasive. Asexual reproduction by suckers (vegetative shoots arising from roots) like some of the weeds have been persistent because they expand the area of coverage where they are present. Seed producers may also become invasive. Monoecious and dioecious species reproduce in different ways. Monoecious plants have separate male and female flowers on the same plant while dioecious plants have male flowers (staminate) on one plant and female flowers (pistillate) on another plant. For species continued existence, the monoeacious plants have an advantage over the dioecious plants. Monoecious plants may be more likely to persist compared to dioecious plants. For animals, from birds, to mammals, to fishes, to all sorts of fauna, there have been reported IAS. Their mode of reproduction range from egg layers to spawners; live bearers and so on, and all have invasive members in their group.

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However, within their groupings, there are reproductive modes which have been more successful than others, e.g. in fish, live bearers over spawners. The production of the next generation is ensured with live bearers. For the batch spawners, there is no guarantee that the eggs they released to the environment will be fertilized and continue to develop.

b. 2. High reproductive rate - fecundity is very relevant to a successful invader. A species with high reproductive rate means that it can produce more seeds (coupled with high germination rate), more eggs, or more offspring every time it reproduces. The species is more likely to have more progeny for the next generation. More progeny means more likelihood of the species being present year after year after year. The species can rapidly increase its population size within a single generation.

b. 3. Presence of parental care - juveniles of species which receive some type of parental care are more likely to grow and develop than those which did not. A large proportion of the young of species without any parental care do not make it to adulthood, compromising the next generation. The presence of some form of parental care, whether it is through bringing food to the young until they can feed themselves, carrying them on their bodies or mouths (like some of the tilapias), guarding the eggs are better than having no parental care at all.

c. Dispersal or Spread - Dispersal or spread may be facilitated by some biological characteristics which we have already discussed above. Specific traits like phenotypic plasticity, fast generation time, and others have also contributed to its spread. Sometimes, size of fruits (small), which may provide a potential food source for species that may pick and carry them with their seeds – thereby expanding the plant’s distribution further. Color of fruits may also make them attractive to other highly mobile animals thus facilitating dispersal. A generalist or opportunistic species also possess a huge advantage in spreading from its distribution.

In addition to the characteristics favoring species invasion, there are other factors which have facilitated them:

d. Human association/affiliation - The species’ importance or desirability to humans have greatly affected species dispersal. Species which are highly ornamental have encouraged it to be propagated in a lot of countries around the world. Agricultural species like vegetables, grains, fruits, livestock, fish and a lot more have been brought outside their native range to benefit humans. We will discuss the different reasons why humans have reshuffled/moved species around the world when we discuss introduction pathways in the next sections. For now, it is important to just remember that most species which have become invasive have been associated with humans.

e. Propagule pressure - Species which have been imported into their non-native ranges in

high numbers are also most likely to have individuals which may escape and establish in the wild compared to those which are imported in low quantities. Examples are fingerlings for aquaculture, seeds for the ornamental industry and so on. Some pathways for introduction are also linked to propagule pressure. This will be discussed in future lessons.

f. History of invasiveness - The history of invasiveness is also an important factor to

consider in assessing the potential of a species to be invasive in a new area. A species which is already known to be invasive in other regions or countries may have a set of characteristics which have enabled it to become invasive, and it is likely that they will become invasive in a new environment. It may not need stringent environmental

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requirements to be able to survive, reproduce and spread. Oftentimes, other members of the genus or family are recognized as invasive.

B. Attributes of successful invaders There are also additional attributes why some species have become successful invaders.

a. Invasive species have traits that favor establishment and spread - Some of those traits

have been presented above, like phenotypic plasticity, high reproductive rate, generalists, and a lot more.

b. They have escaped their natural enemies from the old environment - This is called as

Enemy Release Hypothesis. Some species have grown larger, had higher yield or had generally better performance in their new environment or non-native range. This has been attributed to the fact that when species are imported into the new environments, their predators, competitors and diseases are not imported with them. Lesser predators, competitors and diseases have allowed them to grow faster and larger than their relatives left in their old environment or expand their distributional (with the expansion of their environmental envelope) range. This reallocation of resources is largely related to phenotypic plasticity.

c. Invasive species exploit empty niches (Stachowicz and Tilman, 2005) - Some of the

invasive species were pioneer species. Pioneer species are defined as species which were the first to colonize previously disrupted or damaged ecosystems, beginning a chain of ecological succession that ultimately leads to a more biodiverse steady-state ecosystem. Empty niches are easily colonized because of available resources which could be tapped by the new species, although some extremely rich and biodiverse areas maybe also prone to invasion.

d. Invasive species are favored by anthropogenic pressure and environmental

disturbances on natives (Leger and Espeland, 2010) - Anthropogenic pressure on natives reduces their biotic resistance, it may mean the removal of predators and other possible competitors may facilitate the survival of a new species adjusting to a new environment. Removing the competition increases available resources for a new species, facilitating its establishment.

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Some databases with information on invasive alien species: • CABI Invasive Species Compendium (ISC) www.cabi.org/isc • International Union for the Conservation of Nature (IUCN) http://iucn.org • European Union (EU) www.europa-alien.org • Convention on Biological Diversity (CBD) www.cbd.int/invasive • Global Invasive Species Database (GISD) www.iucngisd.org • Database on Introductions of Aquatic Species (DIAS) www.fao.org/fishery/dias/en • FIshBase http://fishbase.org/search.php • Amphibia Web http://amphibiaweb.org/ • Inter-American Biodiversity Information Network (IABIN) www.oas.org • European Network on Invasive Species (NOBANIS) www.nobanis.org • Mediterranean Science Commission Atlas of Exotic Species in the Mediterranean

www.ciesm.org/online/atlas/ • Global Invasive Alien Species Information Partnership (GIASI Partnership) http://

giasipartnership.myspecies.info/en • Hawaiian Ecosystems at Risk project (HEAR) http://hear.org/ • United States Department of Agriculture (USDA) www.invasivespeciesinfo.gov • United States Geological Society (USGS) http://nas.er.usgs.gov • Global Invasive Species Information Network (GISIN) www.gisin.org

STUDY ACTIVITIES/QUESTIONS 1.3:

By now, you know what attributes and characteristics are associated with invasive alien species. 1.3.1. Continue working on the list of the 10 species you have in SAQ 1-2. Add columns to hold

information on: a. mode or reproduction/propagation b. fecundity c. presence or absence of parental care (for animals) d. environmental tolerances (temp range, salinity range, etc.) e. diet (herbivore, carnivore, omnivore) f. longevity g. growth and maturity data h. importance (used in agriculture, ornamental, etc.) i. competitors or predators.

1.3.2. Select one species (it may be one of your 10 species, as long as you do not select a species

which have been previously selected by another student) which have been identified as non-native to the Philippines. Make a small species profile using the information listed above, provide a picture and a map highlighting where it is found in the Philippines (with references). You will be using the same species for the next reports/assignments.

1.3.3. Some species are able to reproduce via both sexual and asexual means. Would they have

an advantage over species which only have one mode of reproduction? Please justify your answer.

1.3.4. Among the hypotheses which have been proposed as the reason why some alien species

have become invasive, which do you think holds true for your selected species? Why?

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SUGGESTED READING: Department of Environment and Natural Resources-Biodiversity Management Bureau (DENR-BMB). (2017). The National Invasive Species Strategy and Action Plan 2016-2026 (Philippines). Quezon City: Department of Environment Biodiversity Management Bureau and Natural Resources. pp. i-xix, 1-97. REFERENCES: Binggeli, P. 1994. The misuse of terminology and anthropometric concepts in the description of introduced species. Bulletin British Ecological Society 25(1): 10–13.

Bullock, J.M., Hodder, K.H., Manchester, S.J. and Stevenson, M.J. 1997. A review of information, policy and legislation on species translocation, Joint Nature Conservation Committee Report No. 261, Peterborough, 9 pp.

Casal, C.M.V. 2006. Global documentation of fish introductions: The growing crisis and recommendations for action. Biological Invasions. 8: 3-11.

CBD, 2000. Decision VI/23* of the Conference of the Parties to the CBD, Annex, footnote to the Introduction (https://www.cbd.int/doc/handbook/cbd-hb-06-en.pdf).

Copp, G.H., Bianco, P.G., Bogutskaya, N., Erős, T., Falka, I., Ferreira, M.T., Fox, M.G., Freyhof, J., Gozlan, R.E., Grabowska, J., Kováč, V., Moreno-Amich, R., Naseka, A.M., Peňáz, M., Povž, M., Przybylski, M., Robillard, M., Russell, I.C., Stakėnas, S., Šumer, S., Vila-Gispert, A. and Wiesner, C. 2005. To be, or not to be, a non-native freshwater fish? Journal of Applied Ichthyology 21: 242-262.

EU. 2014. Invasive Alien Species: A European Union Response. Brussels, 28 pp.

Falk-Petersen, J., Bohn, T. and Sandlund, O.T. 2006. On the numerous concepts in invasion biology. Biological Invasions 8: 1409–1424.

FAO. 1996. FAO Technical Guidelines for Responsible Fisheries – Precautionary Approach to Capture Fisheries and Species Introductions – 2. Food and Agriculture Organization of the United Nations, Rome, 54 pp.

Godman, A. and Payne, E.M.F. 1986. Longman Dictionary of Scientific Usage. Longman Group Ltd., Harlow, 684 pp.

ICES. 1995. Code of practice on the introductions and transfers of marine organisms 1994/ Code de conduite du CIEM pour les introductions et transfers d’organismes marins 1994. ICES, Copenhagen, 12 pp.

IUCN. 1987. The IUCN Position Statement on Translocation of Living Organisms. International Conservation Union (IUCN), Gland, 11 pp.

IUCN. 1995. IUCN /SSC Guidelines for Re-introductions. IUCN, Gland, 6 pp.

IUCN. 2000. IUCN Guidelines for the Prevention of Biodiversity Loss Caused by Alien Invasive Species. IUCN, Gland, 24 pp.

Jones, C.G., Lawton, J.H. and Shachak, M. 1997. Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78(7): 1946–1957.

Leger, E. and Espeland, E.K. 2010. Coevolution between native and invasive plant competitors. Implications for invasive species management. Evol. Appl. 3: 169-178.

Les, D.H. and Mehrhoff, L.J. 1999. Introduction of nonindigenous aquatic vascular plants in southern New England: a historical perspective. Biological Invasions 1: 281–300.

Lockwood, J.L., Hoopes, M.F., and Marchetti, M.P. 2007. Invasion Ecology. Blackwell Publishing, 304 pp.

Mack, N.M. 2000. Cultivation fosters plant naturalization by reducing environmental stochasticity. Biological Invasions 2: 111–122.

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Mack, R.N. 1996. Predicting the identity and fate of plant invaders: Emergent and emerging approaches. Biological Conservation 78: 107–121.

Morris, C. 1992. Academic Press Dictionary of Science and Technology. Academic Press, San Diego, 2432 pp.

Naylor, R. 1996. Invasions in agriculture: Assessing the cost of the Golden Apple Snail in Asia. Ambio. 25(7): 443-448.

Rainboth, W.I. 1996. Fishes of the Cambodian Mekong. FAO Species Identification Field Guide for Fishery Purposes, FAO, Rome, 265 p.

Randall, J.M. 1996. Defining weeds of natural areas. Pp 18–25 In: Luken J.O. and Thieret, J.W. (eds). Assessment and Management of Plant Invasions. Springer Verlag, New York.

Richardson, D.M., Pyšek, P., Rejmánek, M., Barbour, M.G., Panetta, F.D., & West, C.J. 2000. Naturalization and invasion of alien plants: Concepts and definitions. Diversity and Distributions 6: 93–107.

Stachowicz, J.J. and Tilman, D. 2005. Species invasions and the relationships between species diversity, community saturation, and ecosystem functioning. Pp. 41–64 In: Sax, D.F., Stachowicz, J.J. and Gaines, S.D. (eds). Species Invasions: Insights into Ecology, Evolution, and Biogeography. Sinauer.

Sutinen, J.G. 2000. A framework for monitoring and assessing socioeconomics and governance of large marine ecosystems. NOAA Technical Memorandum NMF S-NE-158, 32 pp.

UKINC (UK Committee for International Nature Conservation). 1979. Wildlife Introductions to Great Britain. Nature Conservancy Council, Peterborough, U.K., 22 pp.

United Nations. 1997. Glossary of Environmental Statistics. Studies in Methods, Series F, No. 67, 83 pp.

Veitch, C. R., Clout, M. N. and Towns, D. R. (eds.) 2011. Island invasives: Eradication and management. Proceedings of the International Conference on Island Invasives. Gland, Switzerland: IUCN and Auckland, New Zealand: CBB. xii + 542 pp.

Wells, M.J., Poyton, R.J., Balsinhas, A.A., Musil, C.F., Joffe, H., Hoepen, E. and Abbott, S.K. 1986. The history of introduction of invasive alien plants to southern Africa. Pp 21–35 In: Macdonald, I.A.W., Kruger, F.J. and Ferrar, A.A. (eds). The Ecology and Management of Biological Invasions in Southern Africa. Oxford University Press, Cape Town.

Williamson, M. 1996. Biological Invasions. Chapman & Hall, London, 244 pp.

WWF. 1976. Reintroductions: Techniques and ethics. Proceedings of the Seminar, Rome, June 1976, 300 pp.

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UNIT 2: PATHWAYS TO INVASION Have you ever seen new plants, insects or animals in your park, school, or backyard? These species may be new to the area or maybe they were already there a few years back but failed to notice them. Maybe you failed to notice them simply because they were few individuals then. Now that they are abundant, they have become more conspicuous and more observable. Alien species invasions begin with one or a few individuals taken from their native range, brought to a new location and released. The transport vector is the means that moves a non-native species into its new location (like boats, planes, etc.), while the transport pathway is the route between the source and release location (e.g. agriculture, biological control, ornamental industry). As global trade continues to increase, so would the movement of species which may establish and become invasive. For an archipelagic country like the Philippines with high species endemism, this would be catastrophic. This section will introduce you to the invasion process, the transport, establishment and spread of alien species. It will try to characterize the early events in the invasion process, the types of transport vectors and pathways and distinguish between intentional and unintentional introductions. Unit 2: Pathways to Invasion

2.1 The Invasion Process 2.1.1. Species Introduction 2.1.2. Intentional Transport 2.1.3. Unintentional Transport 2.1.4. The Philippine Scenario

2.2 Understanding and Predicting Invasion 2.2.1. Major Hypotheses in Invasion Biology 2.2.2. Species Biology and Successful Invaders 2.2.3. IAS and Climate Change

At the end of Unit 2, you should be able to:

Be able to discuss what happens in a species invasion;

Understand why and how species are being moved around the world;

Differentiate vectors against pathways.

2. 1 THE INVASION PROCESS The invasion progress or stages can be divided into four major components: transport, colonization, establishment and spread. Some authors may use different terminologies or further break them down to very specific stages but basically they can be simplified. The transport stage – new species are imported into a country. Invasion always starts with a new species imported into a new country or area. Without these new species entering the country, the other stages of invasion will be none existent. The colonization stage – once the new species has entered and escaped, there are only two things it may do, die or colonize. If the new environmental conditions are favorable to the species or once it acclimatizes to the new environment – the colonization stage is set. The new species acclimatizes and colonizes small pockets of the environment. One may be able to see the species in either one area or a few probably nearby areas.

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The establishment stage – the species have now acclimatized to the new areas they have been able to survive. In order to establish, they should be able to continue their presence in the new environments. This means that they have to propagate or reproduce and ensure the continuity of their species in the new area. After establishing, some species would spread or widen their distribution. This brings us to the spread stage of a species invasion. The species are now found in a lot of places, beyond the initial distribution or introduction area. After some time, a rapid increase in the new species distribution and abundance is observed. This period of time is species and locality specific. Different species have different population doubling times, and species’ population increase are affected by the environment where they are situated. A species in three different environments may increase its number differently based on the existing conditions in the new environments. If the species is allowed to continue its increase and spread, ultimately the invasive species become widespread and abundant. The progression of a species invasion is shown in a simplified diagram below (Fig. 6).

2.1.1. SPECIES INTRODUCTION

In the past, plants may be carried to other nearby or far-flung areas through wind dispersal or by floating to the new areas on ocean currents. However, much has changed as technology has facilitated air and water travel via airplanes and ships. Today, plants and so much more has reached nearby and far-flung areas faster and in huge numbers. Vectors and pathways by which the new species reach the new environments are more diverse and dynamic than the natural colonization patterns.

A. VECTOR OR PATHWAY The transport vector is defined by Mack (2004) as the manner in which species are carried along a pathway, and a pathway as the route between the source region of the non-native species and its location of release. To clarify this, transportation (like a ship, an airplane, a car, humans, animals, etc.) can bring a wide array of items like plants, animals, insects and diseases from one source to many locations – or the HOW they were able to reach their destination. A ship (vector) may move species across regions via ornamental plants (ornamental industry), agriculture, and a lot of other types of species. Hence, a vector may carry non-native species across many pathways.

A pathway is the route between the source region of the non-native species and its location of release – or simply the WHY and WHAT were moved from one place to the next. A pathway may be agriculture, aquaculture, ornamental, pet industry, etc.

TRANSPORT species absent

COLONIZATION

Small number of localized

populations

ESTABLISHMENT

Species reproduce, rapid

increase in abundance

SPREAD

Species widespread and

abundant

Figure 5. The Invasion Process of IAS (Adapted from Casal, 2006)

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B. INTENTIONAL VS. UNINTENTIONAL There are a lot of transport vectors however they can be divided into two major groups: intentional and unintentional introductions.

a. Intentional introductions refer to the movement of species to a new area for a specific

purpose. This includes a wide range of vector categories like the importation of species for food (crop species, livestock, aquatic species, etc.), ornamental (plants, aquarium fishes, etc.), pets (all sorts of species from reptiles to birds to fishes – which may also be ornamental, etc.), biocontrol (fishes, frogs, etc.) and so much more. Since intentional introductions were human-mediated based on human needs and wants, they have been recorded more than unintentional introductions. Records of where (they came from and went to), what (what species have been moved) and when (they have been moved) are available. The information has been lodged in publications, websites and grey literature like student theses/dissertations or government reports all over the world.

b. Unintentional introductions on the other hand refer to the movement of non-native species as secondary results of intentional transfer of other product, good or service. Since these are sometimes not noticeable/apparent/evident, they have remained under the radar and we have very minimal knowledge of these introductions.

2.1.2. INTENTIONAL TRANSPORT

The intentional movement of non-native species is human-mediated borne by human needs and desires. These have been happening since ancient times. Some fruits we enjoy are not native to the Philippines, like the avocado, mango, tamarind, durian, dragon fruit, and a lot more. Some fishes we usually see are not indigenous to the Philippines like tilapia, cream dory or the very popular goldfish (Casal et al., 2007). There are a lot of reasons for moving organisms and a lot of people who do so. Below is a list of reasons behind most of species introductions.

A. AGRICULTURE a. Food source – the earliest species introductions have been correlated to the beginning of

agriculture. In the Philippines, several types of plant species (fruits, vegetables and medicinal plants) have been introduced at the end of the nineteenth century. These came from all over the world. Of these, certain species proved to be valuable, gaining a favorable acceptance among the Filipinos while others were not acceptable to the Filipino palate. Many of the new species relied on humans for their continued propagation, however some have escaped from the confines of the farm, garden, or aquaculture facility and established feral, non-native populations. Some have easily adapted to the tropical conditions of the Philippines with a designated wet and dry season and an average year-round temperature of 26.6°C.

The avocado (Persea americana Mill. 1768) (Family: Lauraceae) is one of these introductions. It is readily accepted by the Filipinos, easily cultivated and is suited to the Philippines climatic condition. The avocado is known as 'abokado' in the Philippine vernacular. It is also called 'aguacate' in Spanish and 'alligator pear', 'Palta pear', 'Midshipman’s butter' in English. It was initially introduced in 1890 by the Spaniards with seeds coming from Mexico. However, it was only when the Americans brought avocado from 1902 to 1907 that it was introduced successfully into the Philippines. Planting materials were received from Hawaii, Costa Rica and the United States through the Bureau of Agriculture. In 1913, the Bureau of Agriculture, together with the College of Agriculture of the University of the Philippines Los Baños, started the countrywide

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spreading of avocado trees. Now, avocados are found growing all over the country, most of which are cultivated in backyards (Sotto, 2000).

b. Forage transported to provide food for animals – some organisms have also been

imported as food for farm animals. In the United States, kudzu (Pueraria montana var. lobata) (Willd.) Sanjappa & Pradeep (Family: Fabaceae) was brought in for forage and as an ornamental plant in 1876. It was planted in a lot of places in the southeastern US but has been recognized as a weed in 1970 (Miller and Edwards 1983). Arachis glabrata Benth. (Rhizoma peanut) (Family: Fabaceae), Arachis pintoi Krapov. & W.C. Greg., 1994 (Pinto peanut) (Family: Fabaceae) and Stylosanthes guianensis (Aubl.) Sw. (Common stylo) (Family: Fabaceae) are not native to the Philippines. However, they are being successfully utilized as forage

crop (Gabunada et al, 1998) in the country. These species as with some other species being utilized in livestock come from the Americas (north to south). Definitely, they have been introduced to the Philippines, when and for what reason remains to be seen. However, the Arachis sp. has also made their presence in the ornamental industry as they make beautiful ground cover.

c. Aquaculture – aquaculture has also been one of the major reasons for species

introduction in the Philippines. To date, over 50 species have been introduced for aquaculture (Froese and Pauly, 2016). Some have escaped the confines of the aquaculture facility. Some of the escapees have established in the wild and formed feral populations. Clarias gariepinus (Burchell, 1822) (African catfish) (Family Clariidae) has been introduced in 1985 from Taiwan (Juliano et al., 1989) and Thailand (FAO, 1997) for aquaculture but has since been more commonly found compared to the native catfish (Clarias macrocephalus Gunther, 1864) Family Clariidae).

d. Established of populations of rare or expensive food items – Rare or expensive species

from other countries are quite expensive if we continue to import them. These enticed some entrepreneurial individuals to bring in these species to plant and propagate them. There are a lot of examples. Lychees or litseyas (Litchi chinensis Sonner, 1782) (Family: Sapindaceae) are not native to the Philippines. They have been introduced in the Philippines by an unknown individual/s and have created an industry which is now booming. Lychee is considered as one of the promising fruit crops of the Cordillera (growing well in Bauko and Bontoc, which has a climate similar to its native distribution) and fetches a relatively high market price. Commercial production is promising. Several varieties are under adaptability trial by Philippine-German Fruit Tree Project at the Bureau of Plant Industry (BPI) in Baguio City include Bangkok, Groff, Albayalde, Kwai mi, Mauritius, Sinco III, Kaimana and UPLB (taken from http://www.pinoybisnes.com/agri-business/lychee-production-guide/).

The golden apple snail (Pomaceae canaliculata Lamarck, 1822) (Family: Ampullariidae) is another species which has been introduced to “increase farmers’ income, enrich the protein in their diet and as aquarium pet” (Joshi, 2007). The idea was for us to culture this as the native species (kuhol) does not reproduce fast enough for the demands of the local market much less for exportation (as escargot). However, as we have seen and experienced, the golden apple snail population has exploded and became a huge agricultural and environmental problem. Economic losses to aquatic crops due to this species are estimated to be up to USD 1,200 million per year (Joshi, 2007).

Figure 6. Arachis sp. in bloom, utilized for forage as well as an ornamental plant.

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B. RECREATION

a. Game species (fishing and hunting) - very little is known about the introduction of game species in the Philippines aside from stories from the Marcos era. Below is an example of one (Box 1).

b. Fishing – the largemouth bass Micropterus salmoides (Lacepède, 1802) (Family Centrarchidae) was introduced to the Philippines by Alvin Seale from California, USA in 1907 for sport (fishing) and as a food fish (aquaculture) (Welcomme, 1988). It was reintroduced in 1915 and 1958 and stocked in Trinidad Lake, Province of Benguet and in Caliraya Lake in Laguna Province. This carnivorous fish has established in Lake Caliraya where it caused the disappearance of some of the original fish of the lake (Sinohin and Cuaterno, 2003).

c. Bait – some species are introduced for bait for fishing. In the US, some introduced species which have been used as bait have very wide distribution. This is because they are brought where fishing is a common activity and facilitated its transport to a broader area. Sometimes the bait escapes the hook and establishes there, other times leftover bait is simply thrown into the lake after fishing. Some of the introductions fail to establish. Other populations have persisted despite heavy harvesting because of repeated releases from private individuals to government agencies and some species do establish self-sustaining populations.

C. ENVIRONMENTAL ENHANCEMENT

Ornamentals – some introductions have been moved to improve natural environments for beauty as well as for cultural satisfaction, this vector category include ornamental and horticultural plants and the importation and breeding of pets. Human migration has facilitated some of these introductions. When people arrive in new environments, sometimes they miss species from their original country or place. They tend to import them and try to grow them in their new environments.

The number of species and individuals transported via this vector is huge. Some 3,290 fish species are used in the ornamental industry (Froese and Pauly, 2016) and over 2,000 species are being traded annually in the ornamental fish trade. Of the ornamental fishes, 90-96% trade volume are coming from freshwaters and usually farm-cultured. Marine ornamental species are usually caught in the wild (Livengood and Chapman, 2007).

Species imported to the Philippines (and some other countries) for the ornamental industry are most often than not remain unreported (Casal, 2015) as these are usually done by private individuals or the pet industry. Hence the data available for this is just the tip of the iceberg. Furthermore, sometimes a particular shipment may consist of other hitchhikers (e.g. none target species).

Figure 7. Micropterus salmoides (Lacepède, 1802) caused the disappearance of some local fishes in Lake Caliraya. Illustration from Eccles 1992.

Figure 8. The janitor fish Pterygoplichthys pardalis (Castelnau, 1855) caught in Laguna. Photo by Rodolfo Reyes, Jr.

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The janitor fish (Pterygoplichthys pardalis (Castelnau, 1855) (Family: Loricariidae) was introduced to the Philippines by the ornamental industry. It has established and had been a huge problem in the early 2000.

BOX 1: INTRODUCTION OF GAME SPECIES IN THE PHILIPPINES

HOW A PATCH OF THE KENYAN WILD ENDED UP IN PHILIPPINES

August 21, 2014 Between May 1976 and February 1977, 102 wild animals were herded into large wooden crates at an undisclosed location in Kenya and bundled onto the overnight cargo train to Mombasa. President Marcos (the then President of the Philippines) was in Kenya in May 1976 to open the 4th United Nations Conference on Trade and Development (UNCTAD). At some point during his stay in Kenya, Ferdinand Marcos made a downpayment of USD 25k of a larger fee of USD 99,250 that would eventually be paid out to Tony Parkinson to capture wildlife for a private safari park Marcos had in mind. In under a year, Parkinson was able to collect 18 impalas, 14 giraffes, 14 zebras, 12 waterbucks, 12 bushbucks, 11 elands, 11 gazelles, and 10 topis which he brought to the Mombasa port. At Kilindini, the animals in wooden crates were transferred onto the open deck of MV Don Salvador III, a cargo ship owned by one of Marcos’s cronies, set out for the small island called Calauit in the Philippines where the now 104 animals in captivity would learn to call home, 9,700 kilometres away from their natural range. Ferdinand Marcos was at hand to receive his African guests ceremoniously releasing one antelope, marking the beginning of an unnecessarily hard life for the animals. Calauit was selected for its isolation which would reduce poaching and disease, allowing the animals to thrive and, in the wisdom of Marcos, that it resembled the African wild and which had been prepared for them since the year before. President Marcos signed the Presidential Proclamation 1578 on August 31, 1976, declaring Calauit a national reserve and relocated the 254 families living there to a new home 40km away. History is unclear over why Marcos went to such trouble to own African animals. His justification was that he loved animals. According to the narrative claims, during the conference, Nairobi begged the International Union for Conservation of Nature (IUCN) for assistance in conserving its diverse wildlife species. President Marcos, in his goodwill, the story goes, established what is today known as the Calauit Safari Park as his modest contribution, however, there is no record of this request. The IUCN actually has a long-standing policy against relocating animals to places that are beyond their natural range. There is another story, a more common unofficial story suggests he established the park for his son Ferdinand Jr. to use as hunting grounds. In an interview in late 2013 with William Mellor of Bloomberg, Ferdinand Jr. disagreed, saying instead “Sure I went hunting, but it was for wild boars that were eating the antelope young. It was never the exotics.’ It could have been the love of a doting father to a spoilt son, or simply the avarice of the ruler. Hunting for wild native boars was worse as he was hunting them to protect the introduced species. Parkinson, remembers a different sequence of events. Months before the conference in Kenya, Ferdinand Marcos and his cronies approached him to do the job - meaning Marcos’ trip to the Eastern African country had other motivations. Parkinson thinks they intended to open a safari park that would be a real-life mini-Serengeti. Ferdinand Marcos wanted some lions and other predators in the park too, but Parkinson dissuaded him. No research was ever done on where they were being relocated to, and what the climate and other conditions were. Papers were signed, and fates sealed. The evicted families began moving back in the 1990s and today, about 1000 people battle for resources with the animals. One giraffe was killed in a conflict with humans, animals have suffered as cyclones and other forms of harsh weather have battered the island. Super Typhoon Haiyan, for example, destroyed their food, putting the herbivores at risk of starvation, it also traumatized the animals and injured nine giraffes and three

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D. ENVIRONMENTAL RESEARCH AND MANAGEMENT Biological control (biocontrol) – a lot of species have been introduced to control other species. There are fishes introduced to control malaria borne by mosquitoes (commonly called mosquito fishes). Mosquito fishes (Gambusia affinis (Baird & Girard, 1853)) (Family:

Poeciliidae) are hardy species, have a short generation time, and are now found in almost any freshwater habitat, including canals, sometimes being the only species found in the area. It has been introduced to the Philippines by Alvin Seale in 1905 (Seale, 1917; Juliano et al., 1989), reintroduced in 1913 and 1920 (FAO, 1997) and is now widely distributed in the country. Rhinella marina (Linnaeus, 1758) (Family: Bufonidae) previously called Bufo marinus has been introduced to the Philippines in the 1930s to control the insect pests in sugar cane fields. Their population has exploded and are now found

everywhere (except in the Palawan island group) thorough subsequent introductions. Among the introduced amphibians, it has exhibited the highest population densities and widest distribution. Although no study on impacts of R. marina has been done in the Philippines, introduced population of R. marina show that the species had adverse ecological impacts on native frog species in other countries (Diesmos, et al., 2006).

E. RESEARCH AND CONSERVATION PURSUITS – in the Philippines, the introduction of several species of wild animals from Kenya presumably in a conservation effort by the then Philippine President Ferdinand E. Marcos between 1976 and 1977 has been documented. Some people have put forward the idea that these were introduced into the island of Calauit to provide hunting as entertainment to his son. In any case, some of the animals established and have increased their populations while some did not make it to the next generation. Now there is a tourism (Africa in Palawan, Calauit Safari) on the island based on the species which have been introduced. (See Box 1.)

2.1.3. UNINTENTIONAL TRANSPORTATION

Some species are inadvertently introduced, as a byproduct of movement of other species or goods. It is difficult to assess these introductions but these are prevalent as evidence shows.

zebras. Inbreeding has become a problem because the animals have been reproducing with the same gene pool for four generations. If unchecked, the lack of diversity will kill off the animals, one species after the other. Calauit Safari Park’s 9,291 acres now host 480 descendants of the Kenyan animals, and about 1,390 local animals. The topi, Thomson’s Gazelle, and the impala species all died out in less than two decades due to poaching and infighting. Poaching remains one of the greatest threats even today. This odd Safari Park was opened to the public in 2009 and is now widely marketed as a mini-Serengeti. As a place where Noah’s Ark left a token. No one associates it with expensive and thoughtless whims, the brutality of its foundation covered up with stories of heroism and compassion. Source: http://owaahh.com/diplomatic-fiasco-how-a-patch-of-the-kenyan-wild-ended-up-in-philippines/

Figure 9. Rhinella marina, an old invasive species in the Philippines. Photo by Arvin C. Diesmos.

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A. SHIP BALLAST One of the best known unintentional introductions is through ballast water. Shipping carries approximately 90% of all internationally traded goods, playing a significant role in world trade. Ballast water stabilizes the cargo ship when it is partly or completely empty. Ballast water prevents heavy rolling and capsizing as well as provide the ship with adequate propulsion, steerage, forward visibility and maximize fuel efficiency. Over 10 billion tons of ballast water are moved around the world annually. Over 10,000 species are transported within ship ballast daily (Carlton, 1999).

When ships fill up their ballast tanks, they take in water surrounding the ship and the organisms living in the water. These unwanted stowaways – marine and freshwater fish larvae and small fish, crustaceans, algae, invertebrates, and even viruses and bacteria – are then let out into a new environment when the ship reaches the next port and discharges its ballast to load cargo. B. CONTAMINANTS

Some species hitchhike with other species, sometimes they have been mixed with other species for aquaculture, like the jaguar guapote (Parachromis managuensis) (Gunther, 1867) (Family: Cichlidae), which was incorporated with tilapia fry and seeds for agriculture. The jaguar gapote was introduced in the Philippines in 1990 (ASAP, 1996). It has been reported to occur in Taal

Figure 10. Ballast water in ships, loading and discharging containing several species from WWF publication. Silent invaders. https://upload.wikimedia.org/wikipedia/commons/2/2a/Ballast_water_en.svg

Figure 11. P. managuensis (Gunther, 1867) is now present in several Philippine waterbodies. Photo by R. B. Reyes, Jr.

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Lake where it has dominated the catch composition of gill nets (Kawit and Rosana, 2002). Significant decline in catch of native species in Taal lake such as Glossogobius guirus (Hamilton, 1822) (Family: Gobiidae), Leiopotherapon plumbeus (Kner, 1864) (Family: Terapontidae) and the Atyid prawn has been attributed to the proliferation of the jaguar gapote (Rosana et al., 2006). In the early 2000, it has been observed in fishermen’s catches in Sampaloc Lake, one of San Pablo’s seven lakes. The theory of how the species got to Sampaloc Lake was that they came in with tilapia fry from Taal Lake, which were stocked into the lake, escaped, established and seemingly outcompeted the local shrimp. The locals took to calling these dugong however they were observed as shrimp catches started to dwindle.

Ticks, mites or fleas and other parasite have hitchhiked on domestic animals or livestock. In a 1997 study of seven plant nurseries in the UK, Hodkinson and Thompson found that 51% of all pots examined contained between one and two hitchhiking plants, species which were not supposed to be there.

2.1.4. THE PHILIPPINE SCENARIO

The workshop on Invasive Alien Species in the Philippines held in 2006 revealed a wide array of species which have been introduced, established and have become invasive in the Philippines. The initial list based on the presentations alone almost reached over 150 species from the terrestrial to the aquatic realm (mammals, birds, plants, fishes, algae, trees, etc.). Of the 100 of the World’s Worst Invasive Alien Species, 17 have been reported from the Philippines. The GISD lists invasive species found in the Philippines, 84 of which are alien, 54 native and 12 of unknown origin. The list is by no means complete. Alien species entered the Philippines through both intentional and unintentional pathways. The table below provides probable pathways of introduction for both aquatic and terrestrial species. These may either be through agriculture or aquaculture, the ornamental or pet industry, as hitchhikers with other species or commodities, or through transportation vectors among others. Prevention and control measures implemented should take into consideration the major pathways identified to be more effective. Pathways of invasion of IAS in the Philippines include those listed in Table 3 below. Table 3. Pathways of Invasion of IAS in the Philippines

1 Intentionally introduced species can also be associated with unintentionally introduced species (pests/hitch-hikers). Intentional introductions

may be both legal and /illegal.

Alien Species Intentional Introductions1 Unintentional Introductions

Aquatic Invasive Species

Aquaculture

Aquarium/Ornamental trade

Biological control

Live bait fish

Live food fish

Stocking

Unauthorized transfer or stocking

Accidental (alone or with other species)

Natural transboundary spread

Ship ballast water management and hull fouling

Water diversions, canals, & dams

Terrestrial

Invasive Species

Agriculture/Horticulture

Game

Live plants & plant parts for propagation

Livestock, poultry, apiculture

Animal products (meat, dairy, eggs, pet food)

Live plants/plant parts for human or animal consumption

Natural transboundary spread

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As global trade continues to increase, so would the movement of species which may establish and become invasive. For an archipelagic country like the Philippines with high species endemism, this would be catastrophic. There is a huge diversity of vectors and the magnitude of their effect on species distribution is not known. This is a good researchable topic to investigate as very few have been studied intensively. We really do not know the magnitude of species being moved around the world or in the Philippines daily, weekly, monthly or yearly. We do not know where they might be coming from, going to or the pathways by which they will be introduced. This is regrettable since the invasion process is heavily influenced by factors expressed during transport. As we go through different sections of this manual and the examples provided, you will see that by targeting the most common pathways of introduction, the influx of alien species will be highly minimized.

2.2. UNDERSTANDING AND PREDICTING INVASIONS

Through time, with the availability of a wider range of transport vectors and pathways, species introductions have exponentially increased. Understanding and predicting invasions or what species might likely become a menace once it is introduced and escapes into the environment is quite difficult as it has to take into consideration extensive and scattered information regarding the species being introduced, the environment where it will or might escape to, the existing species in the environment, the possible interactions it might influence and so on. At the end of this section the student is expected to:

Understand the major hypotheses to explain and predict species invasions,

Know what makes a species a successful invader, and

Understand why climate change facilitates IAS invasion and impacts.

2.2.1 MAJOR HYPOTHESES IN INVASION BIOLOGY Several major hypotheses have been proposed to explain and predict biological invasions but the general applicability of these hypotheses is largely unknown (Jeschke, 2012).

Research & development

Viable seeds & grains

Wildlife/pet trade/zoos (etc.)

With other species

Wood products and other plant products

STUDY ACTIVITIES/QUESTIONS 2.1: 2.1.1. What types of introductions can be easily monitored?

2.1.2 Going back to your list of species, add three more columns and fill up information

pertaining to:

a. type of introduction (intentional, unintentional)

b. vector

c. pathway

Note that there could be more than one type, vector or pathway. Provide references.

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The hypotheses focus on:

Ecosystems into which invaders were introduced (biotic resistance and island susceptibility)

Invaders themselves

Invader-ecosystem interactions

A. BIOTIC RESISTANCE HYPOTHESIS – ecosystems with high biodiversity are more resistant against invaders than ecosystems with low biodiversity. This formulation of the biotic resistance hypothesis is also known as diversity-invasibility hypothesis. This is not limited to invasion biology but also for the question of whether diversity affects ecosystem stability (Ives and Carpenter, 2007).

B. ISLAND SUSCEPTIBILITY HYPOTHESIS – invasive species are more likely to become established and have major ecological impacts on islands than on continents. This hypothesis is related to the biotic resistance hypothesis, as continents typically have higher biodiversity than islands, mainly due to geographic and thus evolutionary isolation. C. INVASIONAL MELTDOWN HYPOTHESIS – the presence of invasive species in an ecosystem facilitates invasion by additional species, increasing their likelihood of survival or ecological impact (Simberloff and Von Holle, 1999). D. NOVEL WEAPONS HYPOTHESIS – in the exotic habitat, invasive species can have a competitive advantage against native species because they possess a novel weapon, i.e. a trait that is new to the resident community of native species and therefore affects them negatively. Prime examples of novel weapons are plant biochemical with allelopathic effects, but traits or other organisms can be considered as novel weapons as well, e.g. toxic substances produced by invasive cane toads (R. marina). E. ENEMY RELEASE HYPOTHESIS – the absence of enemies in the exotic range is a cause of invasion success. If a new (alien) species’ predator or competitor is absent in the new environment, the alien has escaped its enemy. The ‘enemy’ would have controlled its abundance or spread in the new environment. With its absence, it was free to grow, reproduce and spread further. F. TENS RULE – approximately 10% of species successfully take consecutive steps of the invasion process: about 10% of species transported beyond their native range will be released or escape in the wild (they are called introduced species or casuals); about 10% of these introduced species will be able to establish themselves in the wild; and about 10% of species established will become invasive/pest species (Williamson, 1996)

Hypotheses which consider invader-ecosystem interactions have higher empirical support compared to those which only considered only the invaders or the ecosystems and did not include their interactions. Invasional breakdown however had the highest level of support with consistently high levels of support across taxa and habitats (Jeschke, 2012).

2.2.2 SPECIES BIOLOGY AND SUCCESSFUL INVADERS Not all introduced species are ‘bad’ per se. Agriculture has definitely provided us with cultivable and hardy productive species which we have enjoyed like rice, corn, chickens, etc. Most of these are not native to the Philippines. In the same way, not all introduced species establish and not all established species become invasive. That said, managers and decision-makers have to choose which species are allowed to enter the country and even translocated to different ecosystems.

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Species which come from similar environmental conditions (humidity, temperature, climate) have a higher chance of establishing in their new environments. However, similarity of original and new environmental conditions do not necessarily guarantee establishment. An environment with many interacting native or endemic species may also be almost impervious to new entrants. A disturbed or compromised (e.g. polluted, deforested, with invasive species, etc.) environment is more prone to species invasion. Species biological characteristics also play a major role in their establishment and invasion success. There are some traits of species which are more commonly associated with invasives.

A. CHARACTERISTICS OF SUCCESSFUL ANIMAL INVADERS: In his paper in 1989, Erlich provides a list of characteristics which successful invaders. He suggests that successful animal invaders are:

a. Widely distributed (large native range) – abundant in their original range and have high genetic variability. Species with a wide native range allude to a wider environmental tolerance. This means that they may be able to live and thrive in more types of environment. This is also linked to high genetic variability as well as abundance. Some fishes for example are able to thrive from freshwater to saline environments.

b. Adaptable and somewhat opportunistic – able to function in a wide range of physical conditions, have a broad diet, and able to shift between r and K strategy. Species with broad diets can easily establish and thrive in new environments as it would be able to live on whatever is available in the new environment.

c. Vagile or have the freedom of movement – species that are vagile are more successful invaders because they can easily spread to other areas. So species which can spread more easily can expand its range faster in its new ecosystems.

d. Associated with Homo sapiens hence its movement may be facilitated by humans – this usually pertains to species which are utilized by humans, for agriculture, pets, forage and so on. Association with humans is one of the major reasons for deliberate species movement.

e. Have a short generation time or high reproductive rate – species are able to increase population size at a much shorter period of time.

f. Gregarious as opposed to solitary – allowing species to get in contact with mates.

g. Female able to colonize alone

h. Larger than most relatives

All of these have exceptions and indicated by other researchers. Contrary to the belief that the ‘tens rule’ holds for every species introduction, Vander Zanden (2005) mentions that “for vertebrates, approximately one out of four introductions becomes invasive”. This is a very high number – 25%. This definitely emphasizes the looming problem from vertebrate introductions. Marchetti et al., in 2004 proposed that the spread of introduced fishes is best predicted using measures of physiological tolerance and propagule pressure. Meaning the species should have a wide environmental tolerance and are brought in in high numbers. He further puts forward that the species integration and impact are best predicted using a measure of prior invasion success.

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B. CHARACTERISTICS OF SUCCESSFUL PLANT INVADERS In 1992, Mack suggested that there are three major characteristics of plant invaders:

a. They possess characteristics allowing them the opportunity for dispersal (at any spatial scale) – they are utilized as forage, food, fiber, medicine or ornamental or they have been dispersed as a seed contaminant, with animals (attached or within) and in contaminated goods. If they are not considered useful to humans or associated with useful plants – they have practically little opportunity for dispersal.

b. Their dispersal coincides with their escaping their predators, competitors, parasites and pathogens from their point of origin.

c. They have the ability to adapt or tolerate the new environment beyond the point of entry meaning they have a wide environmental tolerance.

It is more useful therefore to look at the biological characteristics of specific known invasives. The data provided here were taken from the websites which are cited as well:

BOX 2: EXAMPLES OF INVASIVE ALIEN SPECIES

Water hyacinth (Eichhornia crassipes)

Distribution: The water hyacinth was originally from tropical South America, but is now found in many warm areas of the world, including the Philippines. Reason for introduction: Introduced around the world via the ornamental trade for aquatic gardens and ponds due to its unusual appearance, attractive flowers, and ability to remove nutrients from the water. Biology: A member of the pickerelweed family (Pontederiaceae), it varies in size from a few centimeters to over a meter in height. It has glossy green, leathery leaf blades up to 20 cm long and 5-15 cm wide and attached to spongy-inflated petioles. Numerous dark, branched, fibrous roots dangle in the water from the underside of the plant. The inflorescence is a loose terminal spike with showy

white, light-blue to violet flowers. Each flower has 6 bluish-purple petals joined at the base to form a short tube. One petal bears a yellow spot. The fruit is a three-celled capsule which contain many minute, ribbed seeds. Reproduction: It reproduces by both sexual (by seeds) and asexual (by budding and stolen production) means. Doubling times have been reported of 6-18 days from stolons while seeds germinate in a few days or remain dormant for 15-20 years. Highly resistant they usually sink and remain dormant during periods of stress (droughts) and upon reflooding, seeds often germinate and renew the growth cycle. Water hyacinths grow over a wide variety of wetland types from lakes, streams, ponds, waterways, ditches, and backwater areas - obtaining their nutrients directly from the water and have been used in wastewater treatment facilities, growing most prolifically in nutrient-enriched waters. New plant populations often form from rooted parent plants. Wind movements and currents help contribute to their wide distribution. Linked plants form dense rafts in the water and mud. Source: (http://www.ecy.wa.gov/programs/wq/plants/weeds/aqua010.html).

Figure 12. Water hyacinth Eichhornia crassipes. Photo by Danilo N. Tandang

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Several protocols are published on risk assessment, usually by taxonomic group as different taxa have different biological characteristics which provide them advantages in establishment and invasiveness. The National Environment Research Council in 2013 evaluated 34 such schemes (NERC, 2013).

2.2.3 CLIMATE CHANGE AND IAS Species distribution is limited by its environmental tolerances. A species will never be found in an environment which does not allow it to grow and reproduce. A species however can expand or shift its distribution based on the changing climate and other factors associated with it. Climate change and invasive species are two of the greatest threats to biodiversity and ecosystem services (Burgiel and Muir, 2010). Climate change and invasive species combined magnifies their biological, ecological and economic impacts. An increase in temperature and CO2 concentrations maybe more advantageous to invasive species due to their adaptability in the face of disturbance,

Mozambique tilapia (Oreochromis

mossambicus (Peters, 1852))

Distribution: the Mozambique tilapia is native to southern Africa and has been introduced and established in over 90 countries including the Philippines. Reason for introduction: It has been widely introduced for aquaculture, but escaped and established itself in the wild in many countries, often outcompeting local species. Aside from aquaculture, it has also been introduced for

sport fishing, stocking man-made lakes and biological control of nuisance plants and animals. Several countries have reported adverse ecological impact after introduction.

Biology: The Mozambique tilapia thrives in a wide variety of environments, from standing waters, reservoirs, rivers, creeks, drains, swamps and tidal creeks; commonly over mud bottoms, often in well-vegetated areas. It also found in warm weedy pools of sluggish streams, canals, and ponds and common in blind estuaries and coastal lakes. It is able to survive extreme reduction of temporary water bodies. Highly euryhaline. It grows and reproduces in fresh-, brackish and seawater and can be reared under hyper-saline conditions. It can tolerate low dissolved oxygen levels and can utilize atmospheric oxygen when water oxygen levels drop. It is mainly diurnal. It is omnivorous, feeding mainly on algae and phytoplankton but also take some zooplankton, small insects and their larvae, shrimps, earthworms and aquatic macrophytes. Juveniles are carnivorous/ omnivorous while adults tend to be herbivorous or detritus feeders. Large individuals have been reported to prey on small fishes, and occasionally cannibalize their own young. It exhibits considerable plasticity in their feeding habits as well as in their reproductive biology. It is a polygamous, maternal mouthbrooder and reaches sexual maturity at 15 centimeter length, but stunted fish may breed at 6-7 centimeters and at an age of just over 2 months. Fecundity is high. It has an extended temperature range 8-42 °C, although its natural temperature range 17-35°C. It can somewhat be aggressive toward other species. An excellent food fish, it is marketed fresh and frozen. It is a most successful and vagile invader. Source: http://fishbase.org/summary/Oreochromis-mossambicus.html. Illustration from Rainboth,

1996.

Figure 13. Mozambique tilapia Oreochromis mossambicus. Figure from Rainboth, 1996.

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enabling higher population growths thereby providing more competition to native species and compromise ecosystem services. Climate change exacerbates the problem of invasive species and as such should also be given attention.

Climate change affects species distributional range, either to constrict, shift or expand it. A new (alien) species entering a new area may be more suited to the modified environment compared to the native species which had suffered stress due to the new climatic condition and hence the alien species will dominate the new area. Species react to stress differently, some adapt others move away or die. Climate change provides varying degrees of stress to different species, making some species’ existence vulnerable in their original environment. Alternatively, IAS can facilitate climatic stress by increasing ecosystem susceptibility to climatic perturbation, through reducing the number of species and their functional types within the ecosystem. In the Philippines, as with other tropical countries, climate change is threatening economic development as evidenced by more frequent and stronger typhoons.

BOX 3: OBSERVED AND PROJECTED CLIMATE CHANGES

Observed

Global average surface temperature increased over the 20th century by 0.74 ± 0.18°C

The years (1995–2006) rank among the 12 warmest years since instrumental records began in 1850.

hot days, hot nights and heat waves have become more frequent while cold days, cold nights and frosts have become less frequent in the past 50 years

Due to the warming pattern, snow and ice extent, including mountain glaciers and snow cover, have decreased

Since the 1970s, area affected by drought has increased

More rain has been observed in eastern North and South America, northern Europe and northern and central Asia while less rain was felt in the Sahel, the Mediterranean, southern Africa and parts of southern Asia

Predicted

There is likely to be warming of 0.2°C per decade in the next two decades

Rate of warming will be greater than any observed during the 20th Century

An increase in global average surface warming by 1.1–6.4°C by 2100 relative to 1980–1999

Global average water vapor concentration and precipitation will increase during the 21st century

Global mean sea level will rise by 18–59 cm between 1990 and 2100 Source: Masters, G.; Norgrove, L. 2010. Climate change and invasive alien species. CABI Working Paper 1,

30 pp

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BOX 4: CLIMATE CHANGE AND IAS AFFECT BIODIVERSITY

Rising temperatures, increased variability of rainfall, greenhouse gas concentrations and frequency and severity of storms and rising sea level will affect invading species, invasive potential and invasability of the host ecosystem. These will act to disturb ecosystems making them vulnerable to invasions, providing opportunities for dispersal and growth of invasive species. IAS must arrive, survive and thrive in their new home and climate change would act on all components of the invasion process. The boundaries for the geographical distribution of species and seasonal conditions for growth and survival are set by climate and landscape features (including land use and land cover). Climate change modifies boundary limits (modifying the climate envelope, climatic space within which a species can survive) and thus would impact the growth, survival and distribution of species. Rising temperatures will have impacts on ecosystems and the species within those ecosystems. However, the magnitude of the impact of the rising temperatures on the species is still unknown. There is a common knowledge however that change in climate may be more conducive to the survival and spread of IAS. IAS may rapidly exploit the niches generated by climatic disturbance and the ecological consequences of climatic disturbance to ecosystems. Prevention measures should thus consider future interactions and synergies where these may increasingly exacerbate the IAS problem. Many invasive alien pathogens will also benefit from climate change as rising average temperatures and shorter and milder winters may promote pathogen growth and reproduction, and potentially higher transmission rates. There would also be indirect impacts of climate change. Warmer shorter winters in cooler temperate regions may stress host species, increasing their susceptibility and benefiting their pathogens. If the pathogen is a biocontrol agent attacking a weed, then the change will be desirable. Generally, net effect maybe negative when one considers drought (changed precipitation patterns) and rising atmospheric carbon dioxide (CO2). Changes will be complex, with weeds and pest animals interacting in many different ways. The distributions of some IAS will change. IAS with short life cycles may evolve rapidly in new locations and escape previous climatic limits. Some species may increase their distributional range while others may find their distribution constricted. Replacement of natives by invasive species will be one of the major impacts of climate change, however changing relationships between predators, pathogens and prey (with either native or introduced species), changing fire regimes, and other climate harm to species already threatened by invasive species may also happen. As invasive species and climate change are considered two of the main threats to biodiversity, the two operating together could be expected to produce extreme outcomes. The combined impacts of IAS and climate change are likely to lead to significantly increased vulnerability of ecosystems and species within them. The changes associated with climate change like elevated CO2, increased temperature, changed precipitation patterns and an increased frequency of extreme events such as fire and flooding will all have significant impacts on ecosystems and IAS. Water is likely to be a key variable which will have the greatest impact on facilitating invasion, particularly through reducing the resistance of agricultural and native ecosystems.

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Generally, IAS, are extremely adaptable to climatic variability. They tend to have rapid dispersal characteristics allowing them to shift ranges in response to changing climatic conditions resulting to them becoming more dominant in many areas. Climate change will disrupt ecosystems with some native species benefiting (directly or indirectly) and some native species declining either directly due to climate change (increased frequency of climate mediated local extinction) or indirectly through altered competitive balances with surrounding species. Some native species may develop invasive tendencies and dominate their habitats. Plants will disperse across the landscape at different rates; it is likely that those arriving ‘first’ may dominate ecosystems and inhibit later arrivals, thus behaving like IAS. Source: Masters, G.; Norgrove, L. 2010. Climate change and invasive alien species. CABI Working Paper 1, 30 pp.

REFERENCES:

(http://owaahh.com/diplomatic-fiasco-how-a-patch-of-the-kenyan-wild-ended-up-in-philippines/) (Accessed January 2015).

ASAP. 1996. Aquarium Database by the Aquarist Society Association Philippines. Data incorporated in FishBase.

Burgiel, S.W. and Muir, A.A. 2010. Invasive species, climate change and ecosystem-based adaptation: Addressing multiple drivers of global ghange. Global Invasive Species Programme (GISP), Washington, DC, US, and Nairobi, Kenya.

Carlton, J.T. 1999. The scale and ecological consequences of biological invasions in the world’s oceans. Pp. 195-212 In: Sundland, O.T., Shei, P.J. and Viken, A. (eds.) Invasive Species and Biodiversity Management. Kluwer Academic, Dordecht.

Casal, C.M.V., Luna, S., Froese, R., Bailly, N., Atanacio, R. and Agbayani, E. 2007. Alien fish species in the Philippines: Pathways, biological characteristics, establishment and invasiveness. Journal of Environmental Science and Management 10: 1-9.

Diesmos, A.C., Diesmos, M.A. and Brown, R.M. 2006. Status and distribution of alien invasive frogs in the Philippines. Journal of Environmental Science and Management 9(2): 41-53.

Eccles, D.H. 1992. FAO species identification sheets for fishery purposes. Field Guide to the Freshwater Fishes of Tanzania. Prepared and published with the support of the United Nations Development Programme (project URT/87/016). FAO, Rome. 145 pp.

STUDY ACTIVITIES/QUESTIONS 2.2:

2.2.1. In all of you selected species, list down what made them successful invaders using a choice or choices of any of the hypotheses and their biological characteristics.

2.2.2 Is the changing climate conducive to the invasion of your selected species? Please explain. By now, you have a lot of information for each of your selected species. Please turn them into

preliminary species profiles.

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Ehrlich, P.R. 1989. Attributes of invaders and the invading process: Vertebrates. Pp. 315-328 In: Drake, J.A., Mooney, H.A., di Castri, F., Groves, R.H., Kruger, F.J., Rejmanek M. and Williamson, M (eds). Biological Invasions, A Global Perspective. Wiley, Chichester.

FAO, 1997. FAO Database on Introduced Aquatic Species. FAO Database on Introduced Aquatic Species, FAO, Rome.

Froese, R. and Pauly, D. (eds). 2016. FishBase. World Wide Web electronic publication. www.fishbase.org, version (01/2016).

Gabunada, F., Magboo, E., Pardinez, V., Cabaccan, C., Castillo, A., Moneva, L., Obusa, A., Asis, P., Mantiquilla, J. and Subsuban, C. 1998. Regional evaluation of forages in the Philippines. In Proceedings of the Third Regional Meeting of the Forages for Smallholders Project held at the Agency for Livestock Services of East Kalimantan, Indonesia. Samarinda, East Kalimantan, Indonesia. 23-26 March 1998. CIAT Working Document No. 188. Edited by W.W. Stür.

Hodkinson, D.J. and Thompson, K. 1997. Plant dispersal: The role of man. J Appl Ecol. 34: 1484-1496.

Ives, A.R. and Carpenter, S.R. 2007. Stability and diversity of ecosystems. Science 31: 58-62.

Jeschke, J.M., Aparicio, L.G., Haider, S., Heger, T., Lortie, C.J., Pyšek, P. and Strayer, D.L. 2012. Support for major hypotheses in invasion biology is uneven and declining. NeoBiota 14: 1-20.

Joshi, R.C. 2007. Problems with the management of the golden apple snail Pomacea canaliculata: An important exotic pest of rice in Asia. Pp. 257-264 In: Vreysen, M.J.B., Robinson, A.S., and Heinrichs, J. (eds). Chapter Area-wide Control of Insect Pests.

Juliano, R.O., Guerrero III, R.D. and Ronquillo, I. 1989. The introduction of exotic aquatic species in the Philippines. In: S.S. De Silva (ed). Exotic aquatic organisms in Asia. Proceedings of the Workshop on Introduction of Exotic Aquatic Organisms in Asia. Asian Fish. Soc. Spec. Publ. 3. Asian Fisheries Society, Manila, Philippines, 154 pp.

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UNIT 3: IMPACT AND MANAGEMENT OF IAS Invasive alien species are one of the top causes for species extinction along with habitat destruction. They have varied and multi layered impacts. These may be direct or indirect impacts. Impacts of invasive alien species can be categorized into four major groups. These are biodiversity, ecosystem services, human health and economic activities. IAS impacts from both the terrestrial and aquatic realm would fall under any of these and may sometimes have more than one impact. Nonetheless, most of these impacts are irreversible, hence the importance of having management plans in place. The management of IAS is actually a mixture of science and plain common sense. It however involves a multidisciplinary approach and multi-sectoral involvement. Management of IAS can also be done on several points, before and after an introduction is made. Pre border control may seem daunting at first but it actually is the most cost effective means of control. At the end of the module, the student is expected to learn:

the types of impacts IAS bring, and

impacts of some IAS in the Philippines

management strategies for addressing IAS

3. 1 IMPACTS OF INVASIVE ALIEN SPECIES

The impacts caused by IAS can be separated into 4 main categories. These are biodiversity, ecosystem services, human health and economic activities. Its impact on Biodiversity includes:

Competition with endemic or native species

Predation on endemic or native species

Transmission of diseases or causing harm to endemic or native species

Hybridization with endemic or native species

Affecting habitats ecosystem engineering or modifying or changing habitats.

For Ecosystem Services (Box 5), recorded impacts include:

Interference with provisioning services

Interference with regulating services

Interference with habitat or supporting services

Interfering with cultural services IAS also impact Human Health and this includes them being vectors of diseases as well as having impacts to the health or the general well-being. Last but not the least, Economic Activities have been impacted by IAS and reported impacts include:

Damage to infrastructures

Damage to landscapes

Damage to agriculture

BiodiversityEcosystem

Services

HumanHealth

Economicactivities

Figure 14. Impacts of IAS

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The major islands of the Philippines have already been invaded by invasive alien species. Leucaena leucocephala (Lam.) de Wit (Family: Fabaceae), Rhinella marina, Pomacea canaliculata, Gambusia affinis, et al. These, among many others are more expensive to eradicate, if at all possible. These are among the invasive alien species that have permanently altered the terrestrial and aquatic ecosystems in the Philippines. A lot of species have been introduced to the Philippines; most of what we see in gardens are non-native species. Some examples are provided below on reported impacts of IAS in the Philippines.

3.1.1 EXAMPLES OF IMPACTS OF AQUATIC IAS

TILAPIA Oreochromis mossambicus - this African species has spread throughout the world via aquaculture but has escaped and established itself in the wild in many countries, often outcompeting indigenous species (Kottelat and Whitten, 1996). It was introduced in the Philippines in 1950 by the Bureau of Fisheries and Aquatic Resources (FAO, 1988 or Welcomme, 1988 ) and has established in brackishwater farms, rivers, lakes, swamps and ricefields throughout the country and caused the near extinction of Mistichthys luzonensis, local called sinarapan, (Smith, 1902) (Family: Gobiidae) (Kottelat and Whitten, 1996). According to Juliano et al, 1989, it competes with the Chanos chanos (Forsskal, 1775) (Family: Chanidae) (milkfish) for food in brackish water farms. Highly inbred, it has hybridized with another introduced species Oreochromis niloticus (Linnaeus, 1758) (Family: Cichlidae) also called tilapia (in the wild and in captivity) (Lever, 1996). This IAS has impacts which include biodiversity

BOX 5: ECOSYSTEM SERVICES

Ecosystem Services are any positive benefits that ecosystems provide to people. These can be direct

or indirect – small or large.

Provisioning Services are ecosystem services that describe the material or energy outputs from

ecosystems. They include food, raw materials, fresh water and other resources (e.g. medicinal).

Regulating Services are the services that ecosystems provide by acting as regulators e.g. regulating

the quality of air and soil, carbon sequestration or storage, moderation of extreme events, waste

water treatment, erosion prevention and maintenance or soil fertility, pollination and biological

disease control.

Habitat or Supporting Services provide everything that an individual plant or animal needs to

survive: food; water; and shelter. This also includes the maintenance of genetic diversity as some

habitats have exceptionally high number of species which makes them more genetically diverse than

others.

Cultural Services are those which include the contribution of the ecosystem to recreation and

mental and physical health (green space); tourism; aesthetic appreciation and inspiration for culture,

art and design; spiritual experience and sense of place.

Source: http://www.teebweb.org/resources/ecosystem-services/

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(hybridize with endemic, compete with native), ecosystem service (provisioning services) and economic activities (lesser yield for the cultured milkfish culture).

KNIFEFISH Chitala ornata (Gray, 1831) (Family: Notopteridae) – The knifefish has been introduced in the Philippines presumably through the ornamental industry. However, it is also considered as a food fish in the Mekong basin, where it is indigenous. It is also utilized in the aquarium industry. In 2007, fishermen began to report its presence in Laguna de Bay. A population explosion was noted shortly after that. The increased abundance of Chitala was accompanied by a decrease in catches of other species, notably the tilapia (another introduced species which has established in the lake but is also being continuously stocked for subsistence fishermen by the government). Gut analyses of the knifefish showed their diet as consisting of other fishes, crustaceans and insects, answering the question why there was a decrease in yield of aquaculture facilities (predation). (Palma, pers. comm.). This IAS has impacts which include biodiversity (prey on native species), ecosystem service (provisioning services) and economic activities (lesser yield for the stocked tilapia in Laguna de Bay).

JANITOR FISH Pterygoplichthys disjunctivus (Weber, 1991) (Family: Loricariidae) Chavez et al., 2006 has reported their presence from Laguna de Bay where they comprised majority of the catch at one time, affecting farmer’s income (Agasen, unpublished). Agasen places date of introduction between 1990-1999. No one knew how it entered the Philippines but the most plausible reason was via the ornamental industry because of its popularity in cleaning fish tanks.

In 2002, an alarming population of janitor fish, P. disjunctivus and P. pardalis, were observed in Laguna de Bay and the tributary rivers (Chavez et al., 2006). This is a common aquarium species feeding on the algae growing on the sides of the aquarium. The escape of janitor fish from cultures along the lakeshore and near the rivers was believed to have caused its introduction. Today, the janitor fish is the most common and abundant aquatic life found in all parts of the lake and some of its more turbid tributaries. Their presence in the area is much more abundant and widespread than those observed in Pasig River. P. disjunctivus may also cause serious environmental and socio-economic impacts in the Agusan Marsh. Their burrowing behavior in river banks may contribute to water turbidity and soil erosion. High water turbidity alters the amount of light that can pass down through the water column, and thus, slows down photosynthesis. This may cause problems in the food web and the energy flow in the marsh ecosystem (Hubilla et al., 2006). This species together with its close relative, P. pardalis (also introduced) creates burrows where it watches over their eggs on the banks of the rivers. This contributes to the siltation and bank erosion and instability. Chavez also reports them as destroying cages and nets causing a decline in native more desirable fish in Laguna de Bay. This IAS has impacts, which include biodiversity (compete with native species for food), and economic activities (lesser yield for the stocked milkfish in Laguna de Bay and damage to infrastructure re bank instability).

Figure 15. Knifefish Chitala ornata in Laguna de Bay. Photo by Cripsina Muan/ Laguna Lake Development Authority

Figure 16. Janitor fish Pterygoplichthys disjunctivus. Photo by Don T. Dumale

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WATER HYACINTH Eichhornia crassipes - the water hyacinth, called the world’s worst aquatic weed, is also present in the Philippines. Its dense growth blocks waterways and inhibits boat traffic, disrupting trade, fishing and recreational activities. The plant is a weed of wetland crops such as rice and jute, and often clogs irrigation canals and pumps, so it also impacts agriculture (GISP, 2008). A free floating aquatic perennial plant. It is abundant in rivers and lakes in the Philippines. Roots intertwine to create floating mats changing the ecosystem. It inhibits light to penetrate thereby decreasing photosynthetic activity, phytoplankton abundance. It decreases algal production, and decreases oxygen levels impacting fishes. This IAS impacts provision of ecosystem services (interferes with provisioning and regulating services (less available O2 for aquatic fauna) cultural services (recreation) and economic activities (agriculture and transportation).

GOLDEN APPLE SNAIL Pomacea canaliculata – The golden apple snail, or locally called golden kuhol, was introduced in the Philippines for the improvement of human nutrition and to serve as an alternative source of income (Halos et al., 2004). However, their escape, establishment and spread have impacted the native Pila luzonica, which was outcompeted by the alien species as well as the rice agricultural sector. Annual losses to rice agriculture in the Philippines from the Golden Apple Snail (GAS) alone has been estimated to cost 28-45 million USD (Naylor, 1996). This IAS impacts biodiversity and economic activities.

3.1.2 EXAMPLES OF IMPACTS OF TERRESTRIAL IAS

IPIL-IPIL Leucaena leucocephala (Lam.) de Wit – The ipil-ipil was introduced as forage into the Philippines from tropical America during the Spanish colonial period. This legume was welcomed at first since it made good firewood and provided shade for understory crops. However, it has escaped cultivation and has become a pest. Exacerbating the problem is that during the American regime, ipil-ipil was among the plants frequently used in the reforestation efforts. During the establishment of forestry and agricultural schools, such as the School of Forestry in Mt. Makiling, Laguna in 1910, L. leucocephala was planted, along with other exotic plants, to afforest the school’s grassy area. It is now considered invasive due to its formation of pure stands which are difficult to eradicate and thus make the land unusable (Baguinon et al., 2005). Clearly, there is a need to re-evaluate the risk management aspects of this plant.

PAPER MULBERRY Broussonetia papyrifera (L.) Vent, 1799 (Family: Moraceae) - Another species which has been introduced is the paper mulberry. No data on its introduction to the Philippines is available but it was introduced at the Makiling Botanic Gardens in the University of the Philippines Los Baños in 1935 (Duran, 2004 as cited by Florece and Colladilla, 2006). This was to augment to vast fiber-producing tree crops in Mt. Makiling. Succeeding introductions were made. It is now widely dispersed around Mt. Makiling and vicinities. It is widely spread in UPLB and in towns and cities outside of UPLB campus such as Bay, Calauan, Calamba City and San Pablo City. Other

Figure 17. The golden apple snail Pomacea canaliculata in a rice paddy. Photo by Ravindra Joshi.

Figure 18. Ipil-ipil Leucaena leucocephala. Photo by Danilo N. Tandang.

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countries are eradicating this species due to its aggressive growth and ability to quickly invade disturbed and abandoned lands. They have become one of the worst plant invaders in Pakistan, Argentina and the USA (Florece and Colladilla, 2006). This IAS impacts biodiversity as it affects the habitats and ecosystem as to disallow/bar other species from growing.

CANE TOAD Rhinella marina – the cane toad was introduced into the Philippines in 1934 from Hawaii to control beetle infestation in sugar cane fields, is now recorded from many major islands. It is confined to the lowlands and medium elevations occupying primarily cleared areas and secondary forests. Although there is no evidence for spatial and resource competition, there is evidence that it competes with these species in terms of breeding sites, depositing its eggs in ponds where some species such as Rana cancrivora, Polypedates leucomystax (Gravenhorst, 1829)(Family: Rhacophoridae) and Kaloula conjuncta (Peters, 1863) (Family: Microhylidae) also lay their eggs. How serious this competition is, is not known. Overall, it may be said that it appears to co-exist ecologically with these three native frog species in the lowlands. The species is considered a trash species. Knowledge of the impact of this species on the native amphibian fauna remains fragmentary (Diesmos et al., 2006). This IAS impacts biodiversity as it competes with indigenous species. COCOLISAP Aspidiotus rigidus Reyne, 1947 (Family: Diaspididae) - One of the most spectacular visually observed impact of an invasive species is the Cocolisap or the Aspidiotus rigidus. It caused so much damage to the coconut industry. Although reports of infestation were already rampant in 2009, the government did not take much notice of this as the infestation was not considered as much of a problem due to the presence of effective natural enemies of a long known. However as time went on, the severity of the outbreak suggested that a different species was responsible for this (Watson et al., 2015). The scale insect encrusts the lower leaf surfaces, blocking the stomata, and stopping photosynthesis: the foliage yellows and dries, fruits form less meat, water inside tastes sour and the tree dies in 6 months or less. CSI-infested trees were trunk injected with systemic insectide (Dinotefuran). Overall, P 177 M was spent for the treatment of CSI-infested trees in 2014. This IAS has biodiversity (transmission of diseases) as well as economic impacts (losses in agriculture dues to death and cost of control).

The estimated cost of the impact of invasive aquatic organisms alone is estimated to be more than 314 billion USD per year in damage and control costs (Pimentel, 2002). Since agriculture accounts for a higher share of the GDP in developing countries, the impact of invasive species on overall economic performance is proportionately greater in developing countries (GISP, 2008). Agriculture related employment accounts for 37% of total employment in the Philippines in 2002 (Daquila, 2005). Thus the impact of invasive species on overall economic performance in a developing country in the Philippines is proportionately greater.

Figure 19. Paper mulberry Broussonetia papyrifera female (left) and male (right). Photo by Danilo N. Tandang.

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Most economic impacts of invasive alien species are not even quantified, e.g.,, in the Agusan Marsh, local fishermen, especially the Manobos, complain that their gill nets are damaged while removing the janitor fish. Destruction of fishing gears subsequently destroys their livelihood. Another problem of the fishermen is that, P. disjunctivus now comprises the bulk of their catch. Target species for gill nets are tilapia (Oreochromis niloticus), common carp (Cyprinus carpio Linneaus, 1758) (Family: Cyprinidae) and giant gourami (Osphronemus gourami Lacepede, 1801). However, they end up catching more janitor fish than their target species (Hubilla et al., 2006). The same can be said in Laguna de Bay and some of the adjacent rivers. Several aquatic animal pathogens/diseases like the Epizootic Ulcerative Syndrome (EUS), White Spot Syndrome Virus (WSSV), and Koi Herpesvirus (KHV) have also entered the country via species importation. These pathogens which entered with other introduced species are a major constraint in the growth of the aquaculture industry (Somga et al., 2002).

3. 2 MANAGEMENT OF INVASIVE ALIEN SPECIES The management of IAS is actually a mixture of science and plain common sense. It however involves a multidisciplinary approach and multi-sectoral involvement. It definitely also involves global and regional instruments. Management of IAS can also be done on several points, before and after an introduction is made. Pre border (before an importation is done) control may seem daunting at first but it actually is the most cost effective means of control. Monitoring, controlling and eradicating are much more costly than prevention. Not only economically but also ecologically because species invasion is irreversible and once a species is lost, it is lost forever. After an invasive species is eradicated or controlled, ecological restoration comes in. This involves four critical components: improving biodiversity conservation, improving human livelihoods, empowering local people and improving ecosystem productivity. At the end of this section, the student is expected to:

Know the types of management actions being utilized to combat IAS and identify which type of management action is best for a particular invasive species.

Know why ecological restoration is an important step in management of IAS

Know the different international and national instruments related to the introduction of IAS

STUDY ACTIVITIES/QUESTIONS 3.1:

3.1.1. Go back to your list of IAS and identify specific impacts or probable impacts these have wrought after their introduction and establishment.

3.1.2. Check out the environment where your IAS are and try to predict which indigenous species

may be impacted. 3.1.3. Take pictures of your species to add to the species profiles you are now preparing. By now, you have accumulated a lot of information for your selected IAS which can be utilized in management and control. 2.2.2 Is the changing climate conducive to the invasion of your selected species? Please explain. By now, you have a lot of information for each of your selected species. Please turn them into

preliminary species profiles.

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3.2.1. ADDRESSING IAS A new IAS in the environment may over time increase in number and widen its distribution. At the same time, and knowing that controlling an infestation is costly as well as impossible if left unabated, the best thing is to have good border control. The goals for addressing the problem of IAS include:

A. PREVENTION

Preventing an IAS from being introduced into a new ecosystem. Ideally, this usually means keeping alien organisms from entering a new country. This is also sometimes termed as pre-border control. Keeping IAS away from any given country is actually the most cost effective way of protecting the ecosystems from any IAS associated problems. This also is the best way to avoid future IAS related problems. This includes a lot of things: legislation, policies, multinational agreements, strict implementation, identification of potential IAS at the border, risk assessments, etc. A list of international and national policies and legislations are provided in this manual (Appendices 1 and 2).

B. EARLY DETECTION Early detection simply means knowing or locating IAS before they have a chance to establish and spread. This usually requires effective, site-based inventory and monitoring programs. Multi stakeholder collaborations are necessary, e.g. government agencies, academe, civil society, etc. Citizen science may also be a good tool to utilize here as government may not be able to be everywhere noticing new entrants into the ecosystem/environment. There are several citizen science activities geared towards IAS detection and monitoring. It is usually the local community which will be able to recognize new species in their nearby ecosystems. When an IAS is detected, management and control costs start accumulating.

C. ERADICATION Eradication means killing the entire population of IAS. Typically, this can only be accomplished when the organisms are detected early. It is extremely difficult to eradicate entire populations of IAS if their presence is widespread and their abundance high. Eradication entails a huge cost depending on the ecosystem invaded as well as the invading taxa. This entails a wide range of methods from mechanical, chemical to biological or possibly combinations of two or even all methods.

D. CONTROL When the IAS population is quite abundant and widespread, it cannot usually be eradicated. The only option at this point is control. Control is the process of long-term management of the IAS’ population size and distribution when eradication is no longer feasible. The wide range of methods utilized in eradication is also utilized here, however, it is clear that the methods, alone or combined may not eradicate the species but may just keep the IAS populations in check. Note that at this stage some of the control measures are recurring, meaning that it is not a one shot thing as these IAS are

Prevention

EarlyDetection

Eradication

Control

43

biological organisms and would be growing and reproducing continuously. Control and eradication methods can take one or more of three forms:

Mechanical control - The physical removal of organisms – pulling weeds, removal of animals like fishing out the janitor fish, for example. The process requires a long-term investment of human and financial resources and course does not always guarantee success.

Chemical control - Chemical control entails the use of chemicals to kill organisms – poisons for wildlife and herbicides for plants, for example. In the Philippines, the cocolisap infestation was curbed with the use of chemicals. Chemical control can be quite costly and typically requires repeat applications.

Biological control – Biocontrol entails the introduction of a highly specific predator, parasite or pathogen that will attack the IAS. This process is not likely to result in eradication of the organism but often can reduce the population of the IAS to tolerable levels. The initial costs associated with research and development may be high, but the long-term costs once applied are low and relatively little maintenance is required. Using local species of biocontrol agents, if possible, is ideal but sometimes the population is not high enough to be able to control the IAS. Precautions should also be taken in introducing a new biological control into an ecosystem so they will not become a future problem.

E. RESTORATION Restoration is the process of re-establishing natural populations and ecosystem functions. In theory, this increases the ecosystem’s resistance to future invasions (Mueller-Dombois, 1981). Although a very important component in IAS management and control, this is more often than not usually overlooked. Management and control without restoration is incomplete as it does not usually lead to sustainability of the ecosystem where IAS have been removed. Without restoration, the ecosystem may still be prone to future invasions.

In all of these, one must remember that when costs escalate as species abundance and dispersal increase. The most cost effective control of IAS is through pre-border control. It is also the only control measure which ensures that an alien species does not have a chance of becoming established and invasive.

Restoration

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3.2.2. MANAGEMENT STRATEGIES AND APPROACHES Preventing and managing IAS are best accomplished through a strategic, holistic approach (Figure 26). International cooperation and capacity building are crucial, as IAS are international problems by their very definition. However, these processes are probably the "weakest link" in any country’s efforts to minimize the spread of IAS. Management takes a lot of forms. In 2007, a review paper by Theoharides and Dukes summarized potential management strategies to reduce the success of invasive species per stage of the invasion process. Tables 4 and 5 are

adaptation of a table from that publication.

Table 4. Potential Management Strategies for Invasive Alien Plant Species Invasion Stage Potential Management Strategies for Plant Species

Transport Regulate plant trade

Promote the use of native species in landscape design

Screen seed stock more effectively for pest or pathogens

Educate the public about the consequences of IAS and the need to prevent their introduction (advocating for native plants in landscape designs, not planting house plants outdoors, etc.)

Colonization Assess species environmental envelope techniques to predict potential range of IAS

Reduce habitat fragmentation and edge effects

Start physical (cutting, mowing) and chemical (herbicide) treatments immediately

Establishment Increase health and seed recruitment of native plants

Promote intact native communities and trophic structure

Study the effects of native (existing) generalist herbivores on IAS for potential control (make sure these species do not prefer natives) and investigate other (native) biocontrols

Reduce human disturbances, promote natural disturbance regime

Continue with the physical (cutting, mowing), and chemical (herbicide) treatments.

Spread Minimize disturbance corridors through natural landscapes

Promote native species that can compete with IAS at the edges of disturbance corridors (e.g. early successional natives)

Isolate source populations of IAS

Eliminate or reduce transport vectors in natural areas during reproductive stage of IAS growth

Prioritize use of local or indigenous practices/techniques to manage colonization and establishment in most susceptible sites to invasion (e.g. sites with high numbers of reproducing individuals, and adjacent sites, sites on the edge of landscapes).

Risk Assessment

& Management

Research

Inventory & Monitoring

Policy & Regulation

Information Management

Education & Outreach

International Cooperation & Capacity

Building

Figure 20. Holistic management of IAS

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For animals, it would be similar as management strategies would follow the same principles.

Table 5: Potential Management Strategies for Invasive Alien Animals

Invasion Stage Potential Management Strategies for Animals

Transport Regulate animal trade

Promote the use of native species in the ornamental industry

Screen fingerlings stock more effectively for pest or pathogens for aquaculture and stocking in natural waters

Educate the public about the consequences of IAS and the prevention of their introduction (not buying nonnative ornamentals, not releasing overgrown pets to the wild, etc.)

Colonization Assess species environmental envelope techniques to predict potential range of IAS

Reduce habitat fragmentation and edge effects

Monitor introduced species (i.e. government agencies or via citizen science)

Start control strategies immediately

Establishment Increase health of native species

Promote intact native communities and trophic structure

Study the effects of native (existing) species on IAS for potential control (make sure these species do not prefer natives) and investigate other (native) biocontrols

Reduce human disturbances, promote natural disturbance regime

Continue with the control strategies

Spread Minimize disturbance of aquatic ecosystems (i.e. habitat modification, pollution, etc.)

Promote native species that can compete with IAS at the edges of disturbance corridors (e.g. early successional natives)

Isolate source populations of IAS

Eliminate or reduce transport vectors in natural areas during reproductive stage of IAS growth

Prioritize use of local or indigenous practices/techniques to manage colonization and establishment in most susceptible sites to invasion (e.g. sites with high numbers of reproducing individuals, and adjacent sites, sites on the edge of the distribution) so spreading of the species are halted.

The strategies mentioned in the tables are just a few examples of how IAS can be managed at different stages of their invasion. There are more strategies which have been applied with varying successes and costs. The strategies are not one size fits all kind but rather they are species-specific, locality-specific and magnitude-specific.

A. COMMONLY PRACTICED MANAGEMENT STRATEGIES In the past, infestation is simply identified as such. There are no qualifiers whether they are introduced or indigenous. One method of controlling pest infestations uses the Integrated Pest Management approach. These can be adapted to invasive species as well.

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BOX 6: EXAMPLE OF AN IAS MANAGEMENT STRATEGY - THE PAMS APPROACH

Adapted from The Practice of Integrated Pest Management (IPM) By Harold Coble, Ph.D.©2003

The practice of IPM is site-specific in nature, with individual tactics determined by the particular crop/pest/environment scenario. There is no one size fits all here. Each site should have in place a management strategy for Prevention, Avoidance, Monitoring, and Suppression of pest populations (the PAMS approach). IPM practitioners utilize at least three of the four PAMS components. The rationale being that success in prevention strategies often make either avoidance or suppression strategies unnecessary.

Prevention is the practice of keeping a pest population from infesting a field or site. It includes using pest-free seeds and transplants, preventing weeds from reproducing, irrigation scheduling to avoid situations conducive to disease development, cleaning tillage and harvesting equipment between fields or operations, using field sanitation procedures, and eliminating alternate hosts or sites for insect pests and disease organisms. Avoidance may be practiced when pest populations exist in a field or site with impact of the pest on the crop avoided through some cultural practice. Examples include crop rotation to break the life cycle of the pest, using cultivars with genetic resistance to pests, using trap crops or pheromone traps, choosing cultivars with maturity dates that may allow harvest before pest populations develop, fertilization programs to promote rapid crop development, and simply not planting certain areas of fields where pest populations are likely to cause crop failure. Prevention and avoidance strategies may overlap in most systems. Monitoring and proper identification of pests, weather monitoring and soil testing can be performed as the basis for suppression activities. Records should be kept of pest incidence and distribution for each field or site to form the basis for crop rotation selection, economic thresholds, and suppressive actions. Suppression of pest populations may become necessary to avoid economic loss if prevention and avoidance tactics are not successful. Suppressive tactics may include Cultural practices such as narrow row spacing or optimized in - row plant populations, alternative tillage approaches such as no-till or strip -till systems, cover crops or mulches, or using crops with allelopathic potential in the rotation. Physical suppression tactics may include cultivation or mowing for weed control, baited or pheromone traps for certain insects, and temperature management or exclusion devices for insect and disease management. Biological controls, Where naturally occurring biological controls exist, effort should be made to conserve these valuable tools.

Prevention Avoidance Monitoring Suppression

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Chemical pesticides are important in IPM programs, and some use will remain necessary. However, pesticides should be applied as a last resort in suppression systems using the following sound management approach: (1) The cost/benefit should be confirmed prior to use (using economic thresholds where available); (2) Pesticides should be selected based on least negative effects on environment and human health in addition to efficacy and economics; (3) Where economically and technically feasible, precision agriculture or other appropriate new technology should be utilized to limit pesticide use to areas where pests actually exist or are reasonably expected; (4) Sprayers or other application devices should be calibrated prior to use and occasionally during the use season; (5) Chemicals with the same mode of action should not be used continuously on the same field in order to avoid resistance development; and (6) Vegetative buffers should be used to minimize chemical movement to surface water.

B. ECOLOGICAL RESTORATION Due to the complexity of the problems in managing, controlling or if possible eradicating IAS, an important component is usually forgotten. This is ecosystem restoration which is most often than not forgotten. The importance of ecosystem restoration is based on the premise that an ecosystem which has been disturbed, damaged or empty may become a playground for new species (sometimes undesirable). ″Ecological restoration is the process of assisting the recovery of an ecosystem that has been degraded, damaged, or destroyed. It is an intentional activity that initiates or accelerates an ecological pathway—or trajectory through time—towards a reference state.″ — Society for Ecological Restoration. Restoration attempts to return an ecosystem to its historic trajectory (SER, 2004). The box below is a summary of what ecological restoration is.

BOX 7. EXAMPLE OF AN IAS MANAGEMENT STRATEGY - ECOLOGICAL RESTORATION

George D. Gann and David Lamb, editors Much of the world's ecosystems have undergone significant degradation with negative impacts on biological diversity and peoples' livelihoods and protecting critical areas alone will not be able to conserve the earth's biological diversity. Ecological restoration should address four elements critical to successful ecosystem management :

Improve biodiversity conservation Improve human livelihoods Empower local people Improve ecosystem productivity

Ecological restoration should be a primary component of conservation and sustainable development program throughout the world. Ecological restoration provides people with the opportunity not only to repair ecological damage, but also to improve the human condition, renew economic opportunities, rejuvenate traditional cultural practices and refocus the aspirations of local communities.

Ecological restoration has as its goal an ecosystem that is resilient and self-sustaining with respect to structure, species composition and function, as well as being integrated into the larger landscape and supporting sustainable livelihoods. Many healthy ecosystems are a product of human endeavors over

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very long time periods and therefore restoration commonly requires the participation of resource dependent communities. In this respect ecological restoration supports conservation and sustainable development efforts worldwide. There are two major challenges involved in undertaking ecological restoration: a.) How to undertake restoration across large areas comprising a variety of land-uses; and, b.) How to equitably balance the trade-offs between improving biodiversity conservation and improvements in human well-being.

Principles of Good Ecological Restoration Practice - Ecological restoration is a well-established practice in biodiversity conservation and ecosystem management. There are fourteen principles of good ecological restoration practice. These principles are consistent with both the scope and intent of the Convention on Biological Diversity’s Principles for the Ecosystem Approach. The principles of good ecological restoration practice are presented in Table 6.

Attributes of Restoration Progress - A degraded ecosystem can be considered to have been restored when it regains sufficient biotic and abiotic resources to sustain its structure, ecological processes and functions with minimal external assistance or subsidy. It will then demonstrate resilience to normal ranges of environmental stress and disturbance. It will interact with contiguous ecosystems in terms of biotic and abiotic flows and social and economic interactions. It will support, as appropriate, local social and economic activities. Such a state is often difficult to achieve. Nevertheless, significant environmental and social benefits can be realized even in the earliest stages of restoration. Restoration can take time before all the benefits are evident. The attributes listed below provide a basis for assessing restoration progress. Some are readily measured, others must be assessed indirectly, including most ecosystem functions, which cannot be ascertained without research efforts that are likely to exceed the capabilities, budgets, and time frames of most restoration projects.

Table 6: Principles of Good Ecological Restoration Practice Good Ecological ration Practice Ecosystems Human Systems

Incorporating biological and environmental spatial variation into the design

Ensuring all stakeholders are fully aware of the full

range of possible alternatives, opportunities, costs and

benefits offered by restoration.

Allowing for linkages within the larger landscape

Empowering all stakeholders, especially

disenfranchised resource users.

Emphasizing process repair over

structural replacement.

Engaging all relevant sectors of society and disciplines,

including the displaced and powerless, in planning,

implementation and monitoring.

Allowing sufficient time for self-generating processes to resume

Involving relevant stakeholders in the definition of

boundaries for restoration.

Treating the causes rather than the

symptoms of degradation.

Considering all forms of historical and current

information, including scientific and indigenous and

local knowledge, innovations and practices.

Include monitoring protocols to allow

for adaptive management.

Providing short-term benefits leading to the

acceptance of longer-term objectives.

Providing for the accrual of ecosystem goods and

services.

Striving towards economic viability

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All of these attributes are not essential to show that good restoration progress is being achieved. It is only necessary for these indicators to demonstrate an appropriate trajectory towards the intended reference ecosystem condition.

Attributes of Accessing Restoration Programs - Attributes may be more specific according to the nature of the restoration goals. For example, one goal may be that the restored ecosystem will provide habitat for rare species or will have a diverse gene-pool for selected species. Yet other goals of restoration may be to provide aesthetic amenities or to accommodate activities of social consequence, such as the strengthening of a community through the participation of individuals in a restoration project. The circumstances that are addressed are often very challenging as areas of degraded ecosystems in various parts of the world are large. Severely degraded ecosystems are costly to repair. Furthermore, many of the degraded ecosystems are continuously used by people of which a majority are poor. Although success in fully eradicating the causes of degradation in these circumstances are not guaranteed there is sufficient evidence from a variety of case studies to be optimistic. It is clear that ecological restoration will be a key element not only of conservation but also for sustainable development worldwide. Restoration can be large-scale or small scale, carried out by one or a few individuals or via government programs involving thousands of participants. It can be well or modestly funded, involve ecosystems that can be restored quickly or those that will require hundreds of years before ecological recovery. In all cases ecological restoration will improve the biological diversity on degraded ecosystems, increase the populations and distribution of rare and threatened species, enhance ecosystem connectivity, increase the availability of environmental goods and services, and contribute to the improvement of human well-being.

Table 7: Attributes of Accessing Restoration Programs Ecosystems Human Systems

The ecosystem contains a characteristic assemblage of the species that occurs in the reference ecosystem and that provide appropriate community structure.

Balance exists between ecological processes and human activities such that human activities reinforce ecological health and vice versa.

The ecosystem contains indigenous species to the greatest practicable extent.

The people who are dependant on the ecosystem have a key role in setting priorities and in project implementation.

All functional groups necessary for the continued development and/or stability of the ecosystem are represented.

Restoration activities are underpinned by economic mechanisms that appropriately assign the costs incurred and equitably distribute the benefits arising at both a local and national level.

The physical environment of the ecosystem is capable of sustaining reproducing populations of the species necessary for its continued stability or development along the desired trajectory.

The ecosystem serves as natural capital that assures a supply of environmental goods and services that are useful to people.

The ecosystem apparently functions normally for its ecological stage of development, and signs of dysfunction are absent.

The ecosystem is suitably integrated into a larger ecological matrix or landscape, with which it interacts through abiotic and biotic flows and exchanges.

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Reference: SER International Primer on Ecological Restoration. www.ser.org. Gann, G.D. and Lamb, D. (eds). 2006. Ecological restoration: A mean of conserving biodiversity and sustaining livelihoods (version 1.1). Society for Ecological Restoration International, Tucson, Arizona, USA and IUCN, Gland, Switzerland.

3. 3 GLOBAL AND NATIONAL POLICIES

3.3.1. GLOBAL, REGIONAL AND NATIONAL LEGISLATION The Philippines as a signatory to international and regional treaties and conventions is duty bound to honor commitments. Appendix 1 presents those related to the introduction of alien invasive species in chronological order, some of which the Philippines have agreed to follow. These cover species in either terrestrial, aquatic or both ecosystems. In the past, focus was only on those which have impacts to agriculture or aquaculture activities. However as global trade and travel increased, so did the entry of new species along with their associated impacts. This necessitated looking at the problem from a wider perspective. The global and regional conventions and agreements were selected from National Invasive Center of the United States Department of Agriculture. https://www.invasivespeciesinfo.gov/laws/intlglobalconv.shtml. Icons were placed beside each treaty or convention to categorize whether it pertains to terrestrial or aquatic ecosystems. Both icons were placed for those covering both terrestrial and aquatic ecosystems. The Philippines responded to international calls to address the invasive alien species problem by drafting legislation and administrative orders. National workshops have also been held to provide a forum for the presentation and discussion of information on invasive alien species (IAS) in the Philippines to contribute to the development of a national strategic framework and action plan on invasive alien species for the Philippines. Appendix 2 presents a list of the legislation and administrative orders related to alien invasive species as the Philippines response to international calls. The different legislation and administrative orders were taken from the Chan Robles Law Library (http://lawlibrary.chanrobles.com) and arranged in chronological order. Icons were placed beside each legislation or administrative order to categorize whether it pertains to terrestrial or aquatic ecosystems. Both icons were placed for those covering both terrestrial and aquatic ecosystems.

Potential threats to the health and integrity of the ecosystem from the surrounding landscape have been eliminated or reduced as much as possible.

The ecosystem is sufficiently resilient to endure the normal periodic stress events in the local environment that are an integral part of the dynamics of the ecosystem.

The ecosystem is self-sustaining. It has the potential to persist indefinitely under existing environmental conditions. Aspects of its biodiversity, structure and functioning will change as part of normal ecosystem development, and may fluctuate in response to normal periodic stress and occasional disturbance events of greater consequence. As in any intact ecosystem, the species composition and other attributes of a restored ecosystem may evolve as environmental conditions change.

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REFERENCES:

Agasen, E.V., Clemente, Jr., J.P., Rosana, M.R. and Kawit, N.S. 2006. Biological investigation of Jaguar

Guapote Parachromis managuensis (Gunther) in Taal Lake, Philippines. Journal of Environmental

Science and Management 9(2): 20-30.

Baguinon, N.T., Quimado, M.O. and Francisco, G.J. 2005. Country report on forest invasive species in

the Philippines. Pp 108-113 In: Philip Mckenzie et. al. (eds). Unwanted Guests: Proceedings in Asia-

Pacific Forest Invasive Species Conference, 17-22 August 2003; Kunming, China: United Nations Food

and Agriculture Organization (UNFAO).

Chavez, J.M., de la Paz, R.M., Manohar, S.K. Pagulayan, S.C. and Carandang VI, R. 2006. New Philippine

record of South American sailfin catfishes (Pisces: Loricariidae). Zootaxa 1109:57-68.

Daquila, T.C. 2005. The economies of Southeast Asia: Indonesia, Malaysia, Philippines, Singapore and

Thailand. Nova Science Publishers, Inc. New York.

Diesmos, A.C., Diesmos, M.L. and Brown, R.M. 2006. Status and distribution of alien invasive frogs in

the Philippines. Journal of Environmental Science and Management 9(2): 41-53.

DOST. 2015. Cocolisap. (http://www.dost.gov.ph/index.php/knowledge-resources/news/44-2015-

news/792-agri-forum-in-dost-s-science-week-reveals-decrease-of-cocolisap-hotspots).

Florece, L.M. and Colladilla, J.O. 2006. Spatial distribution and dominance of Paper Mulberry (Broussonetia papyrifera) in the vicinities of Mt. Makiling, Philippines. Journal of Environmental Science and Management 9(2): 54-65.

Gann, G.D., and Lamb, D. (eds). 2006. Ecological restoration: A mean of conserving biodiversity and sustaining livelihoods (version 1.1). Society for Ecological Restoration International, Tucson, Arizona, USA and IUCN, Gland, Switzerland.

Hubilla, M., Kis, F. and Primavera, J. 2006. Janitor fish Pterygoplichthys disjunctivus in the Agusan

Marsh: A threat to freshwater biodiversity.

STUDY ACTIVITIES/QUESTIONS 3.3:

3.3.1. In your species profiles, add the management protocol which is currently being used for your specific species. Why do you think it will or will not work. Explain.

3.3.2. Knowing what you know now, suggest an alternative or additional management method

to augment the current one being used. 3.3.3. Citizen science is one of the best ways for governments and managers to learn the extent

of species invasion. One of the best ways to encourage citizen participation is through the development of IEC materials. Create a material which could be used to inform people of your selected species.

3.3.4. There are so many International and national legislations and administrative orders re

the introduction of alien species, select one and report about it to the class. 3.3.5 The implementation of these legislation and administrative orders are sometimes not as

good as we would want them to be. Can you suggest how to improve implementation?

By now, you have accumulated a lot of information for your selected IAS which can be utilized in management and control. 2.2.2 Is the changing climate conducive to the invasion of your selected species? Please explain. By now, you have a lot of information for each of your selected species. Please turn them into

preliminary species profiles.

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Joshi, R. C. 2005. Managing invasive alien mollusc species in rice. International Rice Research Notes. 30(2): 5-13.

Juliano, R.O., Guerrero III, R.D. and Ronquillo, I. 1989. The introduction of exotic aquatic species in the

Philippines. Pp. 83-90 In: De Silva, S.S. (ed.) Exotic Aquatic Organisms in Asia. Proceedings of the

Workshop on Introduction of Exotic Aquatic Organisms in Asia. Asian Fish. Soc. Spec. Publ. 3, 154 p.

Asian Fisheries Society, Manila, Philippines.

Kottelat, M. and Whitten, T. 1996. Freshwater biodiversity in Asia, with special reference to fish.

World Bank Tech. Pap. 343, 59 pp.

Lever, C. 1996. Naturalized fishes of the world. Academic Press, California, USA, 408 pp.

Naylor, R. 1996. Invasion in agriculture: Assessing the cost of the golden apple snail in Asia. Ambio 25(7), 443 – 448.

Palma, Adelaida. BFAR. pers. comm.

Rainboth, W.I. 1996. Fishes of the Cambodian Mekong. FAO Species Identification Field Guide for Fishery Purposes, FAO, Rome, 265 pp.

Society for Ecological Restoration International Science & Policy Working Group. 2004. The SER International Primer on Ecological Restoration. www.ser.org & Tucson: Society for Ecological Restoration International.

Somga, J.R., Somga, S.S. and Reantaso, M.B. 2002. Impacts of disease on small-scale grouper culture in the Philippines. Pp. 207-214 In: Arthur, J.R., Phillips, M.J., Subasinghe, R.P., Reantaso, M.B. and MacRae, I.H. (eds). Primary Aquatic Animal Health Care in Rural, Small-scale, Aquaculture Development. FAO Fish. Tech. Pap. No. 406.

Theoharides, K.A. and Dukes, J.S. 2007. Plant invasion across space and time: Factors affecting

nonindigenous species success during four stages of invasion. New Phytologist 176: 256-273.

Watson, G.W., Adalla, C.B., Shepard, B.M. and Carner, G.R. 2015. Aspidiotus rigidus Reyne (Hemiptera: Diaspididae): A devastating pest of coconut in the Philippines. Agricultural and Forest Entomology 17(1): 1–8.

Welcomme, R.L., 1988. International introductions of inland aquatic species. FAO Fish. Tech. Pap. 294.

318 p.

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APPENDICES

Appendix 1. International and Regional instruments related to the introduction of alien invasive

species

Instrument Date and Place

of Adoption

Relevance to the Alien Invasive Species Problem

Terrestrial or Aquatic Realms

The International Plant Protection Convention (IPPC)

1951 (Washington,

USA)

Secures action to prevent the spread and introduction of pests of plants and plant products and promote appropriate measures for their control. https://www.ippc.int/servlet/BinaryDownloaderServlet/13742_1997_English.pdf?filename=/publications/13742.New_Revised_Text_of_the_International_Plant_Protectio.pdf&refID=13742

Plant Protection Agreement for the Asia and Pacific Region

1956 (Rome, Italy)

Compels contracting governments to prevent the introduction into and spread of plant diseases and pests within the South East Asia and Pacific region. (A supplementary agreement under Article III of the IPPC). http://www.fao.org/Legal/TREATIES/006s-e.htm

Convention on Migratory Species of Wild Animals

1979 (Bonn, Germany)

Parties are enjoined “to prevent, reduce or control factors that are endangering or are likely to further endanger the species, including strictly controlling the introduction of, or controlling or eliminating, already introduced exotic species”. Furthermore where required and feasible, the restoration of the habitats of importance, its protection from disturbances, including strict control of the introduction of, or control of already introduced, exotic species detrimental to the migratory species” (Articles 3 and 5). http://www.cms.int/documents/convtxt/cms_convtxt.htm

United Nations Convention on the Law of the Sea (UNCLOS)

1982 Encourages states to take all measures necessary to prevent, reduce and control the intentional or accidental introduction of species, alien or new, to a particular part of the marine environment, which may cause significant and harmful changes thereto (Article 196). http://www.un.org/Depts/los/convention_agreements/convention_overview_convention.htm

The ASEAN Agreement on the conservation of Nature and Natural Resources

1985 (Kuala

Lumpur, Malaysia)

Parties endeavor to regulate and where necessary, prohibit the introduction of exotic species (Article 3 (3c) http://www.aseansec.org/1490.htm

Marine Environment Protection Committee MEPC) of the International

1991 Adoption of the MEPC of voluntary guidelines for preventing the introduction into the marine environment of unwanted aquatic organisms and pathogens from ships’ ballast waters and sediment discharges.

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Instrument Date and Place

of Adoption

Relevance to the Alien Invasive Species Problem

Terrestrial or Aquatic Realms

Maritime Organization (IMO)

Convention on Biological Diversity (CBD)

1992 (Rio de Janeiro, Brazil)

Enjoins parties to “prevent the introduction of, control or eradicate those alien species which threaten ecosystems, habitats or species” (Article 8 (h)). http://www.cbd.int/convention/convention.shtml

Agenda 21-United Nations Conference on Environment and Development (UNCED)

1992 (Rio de Janeiro, Brazil)

Calls for increasing protection of forests from disease and uncontrolled introduction of exotic plant and animal species (11.14); acknowledgment that inappropriate introduction of foreign plants and animals has contributed to biodiversity loss (15.3) http://www.un.org/esa/sustdev/documents/agenda21/english/agenda21toc.htm

United Nations Conference on Environment and Development (UNCED)

1992 (Rio de Janeiro, Brazil)

Requested the IMO to consider the adoption of appropriate rules on ballast water discharge. http://www.un.org/esa/sustdev/documents/agenda21/english/agenda21chapter17.htm

Agreement on the Application of Sanitary and Phytosanitary Measures

1995 A supplementary agreement to the WTO Agreement. Applicable to all sanitary and phytosanitary measures directly or indirectly affecting international trade. http://www.wto.org/english/tratop_e/sps_e/spsagr_e.htm

International Maritime Organization (IMO) 20th General Assembly

1998 “Guidelines for the control and management of ships’ ballast water to minimize the transfer of harmful aquatic organisms and pathogens” (adopted Resolution A.868(20) on) http://www.imo.org/includes/blastDataOnly.asp/data_id%3D22649/A868.pdf

Preventing the Introduction of Invasive Alien Species. Resolution A-32-9. International Civil Aviation Organization (ICAO)

1998 Urges all Contracting States to use their civil aviation authorities to assist in reducing, through civil air transportation, potentially invasive species to areas outside their natural range. Requests the ICAO Council to work with other United Nations Organizations to identify approaches that the ICAO might take in assisting to reduce the risk of introducing potential invasive species

IUCN-Guidelines for the Prevention of Biodiversity Loss Caused by Invasive Alien Species

2000 Guidelines were designed to increase awareness and understanding of the impact of alien species. Provides guidance for the prevention of introduction, re-introduction and control and eradication of invasive alien species http://www.issg.org/infpaper_invasive.pdf

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Instrument Date and Place

of Adoption

Relevance to the Alien Invasive Species Problem

Terrestrial or Aquatic Realms

Cartagena Protocol on Biosafety

2000 (Montreal) The objective of the protocols is to contribute to ensuring adequate level of protection in the safe transfer, handling and use of living modified organisms resulting from modern biotechnology that may have adverse effects on the conservation and sustainable use of biological diversity. http://www.cbd.int/doc/legal/cartagena-protocol-en.pdf

World Summit on Sustainable Development

2002 (Johannesburg,

South Africa)

Called for action at all levels to accelerate the development of measures to address invasive alien species in ballast water. http://www.un.org/jsummit/html/documents/summit_docs.html

Ramsar Convention (8th meeting)

2002 (Valencia, Spain)

Urged contracting parties to address the problems posed by invasive species in wetland ecosystems in a decisive and holistic manner, making use, as appropriate, tools and guidance developed by various institutions and processes, including any relevant guidelines or guiding principles adopted under other conventions (Resolution VIII.18. Invasive species and wetlands) (http://www.ramsar.org/res/key_res_viii_18_e.pdf)

International Convention for the Control and Management of Ships' Ballast Water and Sediments (Ballast Water Management Convention)

2004 Enjoins country signatories to prevent, minimize and ultimately eliminate the transfer of harmful aquatic organisms and pathogens through the control and management of ships' ballast water and sediments. Parties ensure that ballast water management practices do not cause greater harm to their environment, human health, property or resources, or those of other States. http://www.imo.org/conventions/mainframe.asp?topic_id=867

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Appendix 2. National response to International calls

Instrument Date of

Adoption

Relevance to the

Alien Invasive Species Problem

Terrestrial

or Aquatic

Realms

Plant Quarantine Law or Presidential Decree 1433

1978 Passed to address the threat posed by the introduction of species to the environment, particularly its potential impact on agriculture The law specifically regulates the entry of plant, plant products, and animals that may harbor pests or cause harm to agricultural products. http://www.lawphil.net/statutes/presdecs/pd1978/pd_1433_1978.html

Presidential Proclamation 2146

1981 This proclamation considered the introduction of fauna (exotic animals) in public and private forest an environmentally critical project. Any undertaking, which included such activities, will require an Environmental Compliance Certificate (ECC). http://www.tanggol.org/environmental_laws/PROC_2146.html

National Committee on Biosafety of the Philippines (NCBP) Executive Order No. 430

1990 Created the National Committee on Biosafety of the Philippines to formulate national policies and guidelines on biosafety. These policies and guidelines cover work involving genetic engineering as well as activities requiring the importation, introduction, field release and breeding of organisms that are potentially harmful to people and the environment. NCBP reviews and approves work proposals and/or the import and introduction of regulated materials and organisms. Institutions engaged in research, production, manufacture and/or introduction involving potentially hazardous biological work are required to create an Institutional Biosafety Committee which shall be responsible for monitoring its work and enforcing the rules and regulations on biosafety

National Integrated Protected Areas System (NIPAS) Act or RA 7586 NIPAS Act.

1992 Prohibits exotic species for use in the restoration of forests within Protected areas (Chapter 4, Section 10 of its implementing rules and regulations) and the DENR Memorandum Circular 2004-06 which provides the concept of rainforestation farming strategy wherein only indigenous and endemic tree species shall be used as planting materials for forest restoration.

National Biodiversity Strategy and Action Plan (NBSAP)

1997 Sets forth the strategies and actions that the country will pursue to conserve biodiversity. Under the NBSAP, biological pollution due to introduced alien species has been identified as one of the problems and threats to biodiversity and protected areas.

The Philippine Fisheries Code of 1998 (R.A. 8550)

1998 R.A. 8550 bans the introduction of foreign finfish, mollusk, crustacean, or aquatic plants in Philippine waters without a sound ecological, biological, and environmental justification based on scientific studies subject to the biosafety standards. It also requires securing an ECC for activities that may affect the quality of the marine and freshwater bodies. Provided, however, that the Department may approve the introduction of foreign aquatic species for scientific/research purposes (Section 10) http://www.chanrobles.com/republicactno8550.htm

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Instrument Date of

Adoption

Relevance to the

Alien Invasive Species Problem

Terrestrial

or Aquatic

Realms

Wildlife Resources Conservation and Protection Act or RA 9147

2001 The Wildlife Resources Conservation and Protection Act regulates the introduction of exotic wildlife. No exotic species shall be introduced into the country, unless a clearance from the Secretary of the DENR or the authorized representative is first obtained. In cases where introduction is allowed, it shall be subject to environmental impact study, which shall focus on bioecology, socioeconomic and related aspects of the area where the species will be introduced (Section 13). http://www.chanrobles.com/republicactno9147.html

Administrative Order No. 23

26 September

2002

Revised Rules and Regulation on the Importation of game fowls in the Philippines safeguards the local stocks from the introduction of communicable animal diseases possibly introduced through imported animals. http://www.da.gov.ph/n_sub.php?pass=n_agrilaws/AO2002/AO_23.html

Fisheries Administrative Order No. 221

2003 Sets guidelines for the importation of live aquatic animals, non-food fishery products, and microorganisms and biomolecules, including exotic live aquatic animals. It categorizes live aquatic animals based on risk and employs and Import Risk analysis (IRA) System to determine the possible threat of the species to be imported to the endemic species and the environment. The IRA Panel can also recommend temporary suspension of importation of live aquatic animals on a case to case basis based on the existing disease prevalence of the species to be imported. The FAO regulates the importation of live fish and fishery products, aquatic microorganisms and biomolecules including Genetically Modified Organisms (GMO’)s and endangered species subject to the agreement of other agencies concerned. It also defines introduced species (non-indigenous, exotic alien species) as any species intentionally or accidentally transported and released by man into an environment outside its historical or natural range, e.g., goldfish and imported hybrids. The introduction/importation of live fish and fishery products, aquatic microorganisms and biomolecules is prohibited without a valid license/permit issued by BFAR.

Fisheries General Memorandum Order (FGMO) FGMO 078

2003 Restriction of entry of live species importation from Taiwan and China

Fisheries General Memorandum Order (FGMO) FGMO 119

2003 Guideline in the importation of milkfish fry

Administrative Order No. 08

12 March 2003

Rules governing the importation of live cattle from Vanuatu http://www.da.gov.ph/n_sub.php?pass=n_agrilaws/AO2003/AO_08.html

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Instrument Date of

Adoption

Relevance to the

Alien Invasive Species Problem

Terrestrial

or Aquatic

Realms

BFAR’s temporary ban on the importation of Koi and common carp

January 2004

A temporary ban on the importation of Koi and common carp as a precautionary measure to prevent the entry of Koi Herpesvirus (KHV) into the country.

Fisheries General Memorandum Order (FGMO) FGMO 0-04

2004 Selective lifting of suspension of importation of Koi carp

Administrative Order No.16

30 May 2005

Rules governing the importation of live cattle from Brazil

National Biosafety Framework, signed as Executive Order No. 514

2006 Strengthens the National Committee on Biosafety of the Philippines and outlines the roles of various government agencies in the implementation of biosafety–related regulations. It institutionalizes cooperation of various sectors in addressing biosafety problems and is already consistent with provisions of the Cartagena Protocol on Biosafety. Although its scope also covers invasive alien species, the EO focuses primarily on products of biotechnology and applies more to living or genetically modified organisms. One of the reasons that IAS was included in the scope of the order was the lack of a similar national framework that will address this specific problem.

Fisheries Administrative Order No. 225

2007-08 Allowing the importation of the broodstock of Pacific White Shrimp, Penaeus vannamei and the culture of the offspring thereof, Guidelines for the importation and culture of P. vannamei (FAO 225-1); Amendments (FAO 225-2 and 3).

Fisheries Administrative Order No. 230

2009 Allowing the importation and culture of the broodstock and post-larvae of Specific Pathogen Free / Specific Pathogen Resistant (SPF/SPR) Black Tiger Shrimp, Penaeus monodon and the culture of the offspring thereof; Guidelines for the importation and culture of P. monodon (FAO 230-1).

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ACKNOWLEDGEMENTS The Invasion Biology Course Manual was developed as part of the United Nations Environment

Programme-Global Environment Facility (UNEP-GEF) Project No. 0515: Removing Barriers to Invasive

Species Management in Production and Protection Forests in Southeast Asia (FORIS Project).

FORIS Project-Philippines National Steering Committee:

Ernesto D. Adobo, Jr., Undersecretary for Administration and Information Systems, Department of

Environment and Natural Resources (DENR)

Rommel R. Abesamis, Assistant Secretary, Department of Environment and Natural Resources (DENR)

Edwin G. Domingo, Director, Foreign Assisted and Special Projects Office Department of Environment

and Natural Resources (FASPO-DENR)

Theresa Mundita S. Lim, Director, Biodiversity Management Bureau, Department of Environment and

Natural Resources (BMB-DENR)

Henry A. Adornado, Director, Ecosystems Research and Development Bureau, Department of

Environment and Natural Resources (ERDB-DENR)

Ricardo L. Calderon, Director, Forest Management Bureau, Department of Environment and Natural

Resources (FMB-DENR)

Juan Miguel T. Cuna, Director, Environmental Management Bureau, Department of Environment and

Natural Resources (EMB-DENR)

Paz J. Benavidez, Assistant Secretary, Bureau of Plant Industries, Department of Agriculture (BPI-DA)

Leonardo M. Javier, Jr., League of Municipalities of the Philippines (LMP)

Datu Tungko M. Siakol, Regional Director, DENR Region XII

Jose Andres A. Canivel, Executive Director, Philippine Tropical Forest Conservation Foundation, Inc.

(PTFCF)

FORIS Project-Philippines Technical Working Group:

Josefina L. de Leon, BMB-DENR

Carmelita I. Villamor, PhD, ERDB-DENR

Cristina M. Regunay, FASPO-DENR

Elma M. Eleria, FASPO-DENR

Ma. Alma P. Segui, FASPO-DENR

Genesis J. Francisco, FMB-DENR

Raul M. Briz, FMB-DENR

Rebecca B. Aguda, FMB-DENR

Consolacion P. Crisostomo, EMB-DENR

Marivic E. Yao, EMB-DENR

Anson M. Tagtag, BMB-DENR

Nermalie M. Lita, BMB-DENR

Cecille G. Francisco, BMB-DENR

Leonardo M. Florece, PhD, University of the Philippines Los Baños (UPLB)

Wilma R. Cuaterno, BPI-DA

Edwin R. Tadiosa, PhD, National Museum of the Philippines (NMP)

Danilo N. Tandang, NMP

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Project Coordinating Unit:

International Project Coordinating Unit: Annamalai Sivapragasam, PhD, Hong Twu Chan, and Arne

Witt, PhD/Centre for Agriculture and Bioscience International (CABI)

National Project Coordinating Unit: Wildlife Resources Division, BMB-DENR

National Project Director: Theresa Mundita S. Lim, DVM

National Project Coordinators: Rheyda P. Hinlo-Arguelles, DVM (2012), Marianne P. Saniano (2013),

and Cynthia Adeline A. Layusa-Oliveros (2015)

National Project Administrators: Ma. Fe Cristobal (2012), Rosene M. Balatibat (2015)

Project Assistants: Flordeliza L. De Leon, Jennifer N. Caisip

Invasion Biology Course Manual Contributors:

Technical Writer and Consultant: Christine V. Casal, Ph.D.

Technical Reviewers: Leonardo M. Florece, Ph.D., Arne Witt, Ph.D., Annamalai Sivapragasam, Ph.D.

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