Sardinella Tawilis, Bombon Sardine Errata Version Assessment By: Hata, H., Santos, M., Di Dario, F., Munroe, T.A., Torres, F., Quilang, J.P

Home , Balayan Bay, Harengula, Sardinella, Sardinella tawilis, Taal Lake, Taal Volcano

The IUCN Red List of Threatened Species™ ISSN 2307-8235 (online) IUCN 2008: T98836352A143839946 Scope: Global Language: English

Sardinella tawilis, Bombon Sardine Errata version Assessment by: Hata, H., Santos, M., Di Dario, F., Munroe, T.A., Torres, F., Quilang, J.P.

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Citation: Hata, H., Santos, M., Di Dario, F., Munroe, T.A., Torres, F., Quilang, J.P. 2018. Sardinella tawilis (errata version published in 2019). The IUCN Red List of Threatened Species 2018: e.T98836352A143839946. http://dx.doi.org/10.2305/IUCN.UK.2018- 2.RLTS.T98836352A98886655.en

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THE IUCN RED LIST OF THREATENED SPECIES™ Taxonomy

Kingdom Phylum Class Order Family

Animalia Chordata Actinopterygii Clupeiformes Clupeidae

Taxon Name: Sardinella tawilis (Herre, 1927)

Synonym(s): • Harengula tawilis Herre, 1927

Common Name(s): • English: Bombon Sardine, Freshwater Sardinella Taxonomic Source(s): Eschmeyer, W.N., Fricke, R. and Van der Laan, R. (eds). 2016. Catalog of Fishes: genera, species, references. Updated 1 July 2016. Available at: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. (Accessed: 1 July 2016).

Taxonomic Notes: Sardinella tawilis is the only freshwater species of Sardinella and is closely related to the marine sister- species, S. hualiensis (Willette et. al. 2014). A recent genetic study indicates that S. tawilis diverged from S. hualiensis in the late Pleistocene, prior to the formation of Taal Lake in the 18th century (Willette et al. 2014). Assessment Information

Red List Category & Criteria: Endangered A2bd; B1ab(iii,v)+2ab(iii,v) ver 3.1

Year Published: 2018

Date Assessed: February 28, 2017

Justification: Sardinella tawilis, a freshwater, lacustrine species, is endemic to a single lake location in the Philippines (Taal Lake). Its Area of Occupancy (AOO) is less than 244 km2 and its Extent of Occurrence (EOO) is 297 km2. Within Lake Taal, there are major threats to fish diversity and this species due to overexploitation, pollution and competition and/or predation with introduced fishes, resulting in continuing declines in habitat quality and number of mature individuals. It therefore qualifies for Endangered under criterion B1ab(iii,v) and B2ab(iii,v). Furthermore, catches of this species have declined significantly since at least 1998, and it is estimated that harvest has declined by about 49% over the past 10 years (more than three generation lengths). Fishing effort using illegal gears which target this species in the lake is increasing, but at this time the rate of increase has not been quantified specifically, so it is inferred that the population has declined by at least 50% over the past 10 years, which qualifies it for Endangered under criterion A2bd. Therefore, S. tawilis is listed as Endangered under A2bd, B1ab(iii,v), B2ab(iii,v). This species, and Taal Lake, are considered high priorities for conservation by the Philippine government.

Range Description: This species is endemic to a single location in the Philippines: Lake Taal (formerly Lake Bombon: Whitehead 1985, Papa et al. 2008). The area of the hydroshed which Lake Taal is within is estimated as 258 km2. Since there is a large island (Volcano Island) within this lake, the AOO of this aquatic species is less than 258 km2. The lake has a surface area of 244 km2 (Mutia et al. 2001, Papa et al. 2008). Its EOO, which is calculated as the area of the minimum convex polygon drawn around the hydroshed of the lake, is estimated at 297 km2. The deepest depth of the lake is 200 m, but this species likely occurs only in the upper 50 m. Based on the major threats to this species (ongoing pollution and invasive species), S. tawilis occupies a single location.

Country Occurrence: Native: Philippines

© The IUCN Red List of Threatened Species: Sardinella tawilis – published in 2018. 3 http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T98836352A98886655.en Population This species is the most dominant fish species caught in Taal Lake. Since 1998, there has been a steady decline in the catch of this commercially important fish attributed to overfishing, illegal use of active fishing gears such as motorized push net and ring net, proliferation of fish cages, and deterioration of water quality (Mamaril 2001, Mutia et al. 2004, Mutia et al. 2011, Quilang et al. 2011, Mutia 2015). The introduction of several species of non-native piscivores (e.g., Oreochromis niloticus, Sarotherodon melanthoron) for commercial purposes has contributed to the decline of Sardinella tawilis stocks (Villanueva et al. 1996, Mamaril 2001, Mutia 2015). A survey conducted from 1996 to 1999 recorded 27 fish species from 32 families in the lake, which is much lower than records from the 1920s that recorded 101 species from 32 families. Given this, about 87% of fish species had disappeared by 1996, which coincided with the same period that aquaculture began (Mutia et al. 2001).

Harvest of this species has been declining since about 1998, when harvest was about 1,672 mt (Mutia et al. 2011). Given the maximum age of this species (3 years), the generation length is less than 3 years, and thus the time window over which declines should be measured is 10 years (2007-2017). Data are not available for every year since 1998, so an exponential regression was run on the data that we do have. The harvest in 2005 was estimated to be about 240 mt, and the last year for which we have data (2010) was about 107 mt: (Mutia et al. 2011), resulting in an decline of approximately 80 % over the past 10 years (2007-2017). However, the harvest appears to be relatively stable since 2011 (M. Santos pers. comm. 2017). If the 107 mt harvest estimated in 2010 is applied to 2017, the resulting decline would be about 49% over the past 10 years (2007-2017).

In general, total fishing effort has decreased since 1998, measured by the number of fisherfolk, boats, and gear types used which has decreased by 16%, 7% and 39%, respectively (Mutia et al. in press). Although there are some management measures in place (e.g., restricting gears), it is inferred that the fishing effort for this species is increasing; the use of illegal active gears (e.g., motorized push net, beach seine and ring net) which largely target this species has been increasing in the most recent 14 years available (1998 - 2011), while catch of this species has declined. The rate of increase of fishing effort is unknown; however, when effort is stable, catch can be a reasonable proxy for the population, and we would infer that the population decreased by about 49% over the past 10 years. With an increase in effort, it is likely that the population is declining faster than the catch, and we therefore infer that the population has declined by at least 50%, which qualifies for Endangered under criterion A2.

Despite records of a decline in fishery landings, this species remained a dominant species taken in Lake Taal fisheries year round (represented 39.2 % of total production in 2010); high reported catches are mostly attributable to the illegal use of active fishing gears (e.g., motorized push net, beach seine and ring net) during months of peak abundance (Mutia et al. 2011). Current Population Trend: Decreasing

Habitat and Ecology (see Appendix for additional information) This is a freshwater, lacustrine species. It is the only species of Sardinella known to occur exclusively in freshwater. Taal Lake is an oligotrophic lake with a maximum depth of 180 m that drains through the Pansipit River into Balayan Bay to the southwest (Papa et al. 2008). This species feeds mainly on copepods and small amounts of cladocerans and rotifers (Papa et al. 2008). Peak spawning is between

© The IUCN Red List of Threatened Species: Sardinella tawilis – published in 2018. 4 http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T98836352A98886655.en either March and May or May and July (Aypa et al. 1991, Joson-Pagulayan 1999). In general, sexual maturity is obtained at 11.2 cm total length (TL: male) and 11.6 cm TL (female); however, it was observed that individuals can mature as early as 8.5 cm TL (Mutia 2015). Spawning females produce approximately 18,000 eggs per spawning season (Mutia 2015). Its body weight ranged from 4.6 g to 35.9 g and its maximum total length is about 15.6 cm (Mutia 2015). The maximum age is about three years, and therefore the generation length must be less than three years.

Systems: Freshwater

Use and Trade This is a dominant fish species caught in Taal Lake. It has been ranked first in landings since 1996 with the highest annual fishery production recorded at 1,120 metric tons in 1998 (Mutia et al. 2001). In a survey conducted from 1996 to 2000, 57% of the total fish landings in Taal Lake consisted of Sardinella tawilis (Mutia et al. 2005 via Quilang et al. 2011). Despite records of a decline in fishery landings, this species remained a dominant species taken in Lake Taal fisheries year round (represented 39.2 % of total production in 2010); high reported catches are mostly attributable to the illegal use of active fishing gears (e.g., motorized push net, beach seine and ring net) during months of peak abundance (Mutia et al. 2011).

The highest average CPUE of all gears was the motorized push net (544.3 kg/day), which is the main gear used to target this species (Mutia et al. 2011). Average CPUE for ring net, beach seine and gill net were 30 kg/day, 25.6 - 29 kg/day and 5 - 6.6 kg/day, respectively (Mutia et al. 2011, Mutia 2015). Seasonal occurrence of this species impacts market price; for example, during May - June when this species is abundant, market price ranged from P40 - 120 / kg and October - January when this species is less abundant, market price increased to P180 - 220 / kg (Mutia et al. 2011). The most recent exploitation rate was estimated to be 0.69, which is similar to reported estimates in previous studies (e.g., 0.62 in 1994 - 1995: Villanueva et al. 1996 and 0.59 in 2000: Mutia et al. 2004). The most recent data available suggest that a total of 257 fisherfolk target this species specifically representing roughly 11.2 % of total fisherfolk (Mutia et al. 2015).

Threats (see Appendix for additional information) The ongoing major threats to this species include overexploitation, pollution, habitat degradation and competition from species introduced for aquaculture (Villanueva et al. 1996, Mamaril 2001, Mutia et al. 2001, Papa et al. 2008, Quilang et al. 2011). It is heavily exploited in mixed fisheries. In 2008-2009, the estimated fishing mortality was 1.93 and the exploitation rate was 0.56, suggesting that the species was overexploited (Mutia et al. 2011). Taal Lake is subject to pollution from aquaculture feeds, domestic waste, and unmanaged tourism on Volcano Island. Aquaculture facilities in Taal Lake have caused habitat destruction and hampered the movement of this species. Competition and/or predation by introduced aquaculture fishes are likely occurring.

Conservation Actions (see Appendix for additional information) Taal Lake has been listed as a conservation area of extremely high importance that is in urgent need of further research (Papa et al. 2008). It has been listed as a protected seascape (Taal Volcano Protected Landscape) and is administrated by a Protected Area Management Board. As a result, there has been a reduction in the number of fish cages in the lake by ~50% (M. Santos pers. comm. 2017).

© The IUCN Red List of Threatened Species: Sardinella tawilis – published in 2018. 5 http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T98836352A98886655.en The local government currently implements national policy of open access in municipal fisheries (Mercene-Mutia 2001). Conservation strategies in the lake have attempted to protect this species from overfishing (Mamaril 2001). For example, motorized push-nets and beach seines have been banned throughout the entire lake (M. Santos and J. Torres pers. comm. 2017). However, despite local laws which ban active fishing gears (e.g., motorized push nets, beach seines and ring nets), these measures are still being used and effort has increased in the most recent years available (1998 - 2014: Mutia et al. 2011). Therefore, it is recommended that local government agencies should be more active in the implementation of various laws on lake management and conservation (Mutia et al. 2011).

Attempts to protect the spawning population and habitat of this species are in place; a Tawilis Reserve Area (TRA) was established in Lake Taal under the Unified Rules and Regulations on Fisheries of Taal Volcano Protected Landscape (URRF-TVPL); in the TRA, only passive and traditional fishing gears like gill net, spear gun and hook and line are allowed (Mutia et al. 2016). Currently, spawning area closures are planned but have not yet been implemented pending completion of scientific research (M. Santos and J. Torres pers. comm. 2017). In addition, translocation to Lake Lanao in Mindanao, Philippines has been considered (Mamaril 2001), but there is no action plan at this time. Credits

Assessor(s): Hata, H., Santos, M., Di Dario, F., Munroe, T.A., Torres, F., Quilang, J.P.

Reviewer(s): Birge, T.L., Ralph, G.

Facilitators(s) and Ralph, G. Compiler(s):

© The IUCN Red List of Threatened Species: Sardinella tawilis – published in 2018. 6 http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T98836352A98886655.en Bibliography Aypa, S., Galicia Jr, A. and Lapasaran, E.S. 1991. A contribution to the biology of Harengula tawilis in Taal Lake, Batangas. Bureau of Fisheries and Aquatic Resources Completion Report to the Department of Agriculture, Bureau of Agricultural Research. Quezon City.

IUCN. 2018. The IUCN Red List of Threatened Species. Version 2018-2. Available at: www.iucnredlist.org. (Accessed: 15 November 2018).

IUCN. 2019. The IUCN Red List of Threatened Species. Version 2019-1. Available at: www.iucnredlist.org. (Accessed: 21 March 2019).

Joson-Pagulayan, A.E. 1999. Aspects of the reproductive biology of the Sardinella tawilis. University of the Philippines.

Mamaril, A.C. 2001. Translocation of the clupeid Sardinella tawilis to another lake in the Philippines: a proposal and ecological considerations. In: Santiago, C.B., CuvinAralar, M.B. and Basiao, Z.U. (eds), Conservation and Ecological Management of Philippine Lakes in relation to Fisheries and Aquaculture, pp. 133-147. Quezon City.

Mercene-Mutia, M.T. 2001. Assessment of local government's implementation of open access policy in Taal Lake, Philippines: Effects on lake conservation and management. In: Santiago, C.B., Culvin-Aralar, M.L., and Basiao, Z.U. (eds), Conservation and Ecological Management of Philippines Lakes in Relation to Fisheries and Aquaculture, pp. 123 - 132. Southeast Asian Fisheries Development Center, Aquaculture Department, Iloilo, Philippines; Philippine Council for Aquatic and Marine Research and Development, Los Banos, Laguna, Philippines; and Bureau of Fisheries and Aquatic Resources, Quezon City, Philippines.

Mutia, M.A.T.M. 2015. ENVIRONMENTAL INFLUENCES ON THE REPORDUCTIVE BIOLOGY AND POPULATION DYNAMICS OF SARDINELLA TAWILISIN LAKE TAAL, PHILIPPINES. Department of Environmental Sciences, University of the Philippines Los Banos.

Mutia, M.T., Magistrado, L. and Muyot, F. 2001. Assessment of Lake Taal fisheries. Taal, Batangas, the Philippines. National Fisheries Biological Centre: 1-17.

Mutia, M.T.M., Muyot, C.M., Torres, F.B. Jr. and Faminialagao, C.M.. In: Lakecon 2011: Building on the pillars of Integrated Lake Basin Management (Second National Congress on Philippine Lakes). Aralar MLC, Borja AS, Palma AL, Mendoza MM, Ocampo PC, Manalili EV, Darvin LC, eds. Los Baños, Laguna: PCARRD-DOST, 2013. (Summary of Proceedings No. 1/2013). 337p. 2013. Seasonality, abundance and biology of “Tawilis” (Sardinella tawilis) in Taal Lake, Batangas. Lakecon 2011: Second National Congress on Philippine Lakes: 337. Los Baños, Laguna.

Mutia, T.M., Magistrado, M.L. and Muyot, M.C. 2004. Status of Sardrinella tawilis in Taal Lake, Philippines. 8th ZONAL Center II Research and Development Review. De La Salle, University, Taft, Manila.

Papa, R.D.S., Pagulayan, R.C. and Pagulayan, A.E.J. 2008. Zooplanktivory in the Endemic Freshwater Sardine, Sardinella tawilis (Herre 1927) of Taal Lake, the Philippines. Zoological Studies 47(5): 535-543.

Quilang, J.P., Santos, B.S., Ong, P.S., Basiao, Z.U., Fontanilla, I.K.C. and Cao, E.P. 2011. DNA barcoding of the Philippine endemic freshwater sardine Sardinella tawilis (Clupeiformes: Clupeidae) and its marine relatives. The Philippine Agricultural Scientist 94(3).

Villanueva, L.S., Luistro, A.P. and Calabig, C.S. 1996. Assessment of Lake Taal capture fisheries with emphasis on the exploitation of Harengula tawilis. Tanauan, Batangas, the Philippines. STIARC- Experimental Farm for Fisheries.

Whitehead, P.J.P. 1985. Clupeoid fishes of the world (suborder Clupeioidei). An annotated and illustrated

© The IUCN Red List of Threatened Species: Sardinella tawilis – published in 2018. 7 http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T98836352A98886655.en catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies and wolf-herrings. Part 1 - Chirocentridae, Clupeidae and Pristigaste. Food and Agricultural Organization (FAO), Rome, Italy.

Citation Hata, H., Santos, M., Di Dario, F., Munroe, T.A., Torres, F., Quilang, J.P. 2018. Sardinella tawilis (errata version published in 2019). The IUCN Red List of Threatened Species 2018: e.T98836352A143839946. http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T98836352A98886655.en

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Habitats (http://www.iucnredlist.org/technical-documents/classification-schemes)

Major Season Suitability Habitat Importance? 5. Wetlands (inland) -> 5.5. Wetlands (inland) - Permanent Freshwater Resident Suitable Yes Lakes (over 8ha)

Threats (http://www.iucnredlist.org/technical-documents/classification-schemes)

Threat Timing Scope Severity Impact Score 5. Biological resource use -> 5.4. Fishing & harvesting Ongoing Unknown Rapid declines Unknown aquatic resources -> 5.4.2. Intentional use: (large scale) [harvest] Stresses: 2. Species Stresses -> 2.1. Species mortality 7. Natural system modifications -> 7.3. Other Ongoing Unknown Unknown Unknown ecosystem modifications Stresses: 1. Ecosystem stresses -> 1.2. Ecosystem degradation 2. Species Stresses -> 2.2. Species disturbance 8. Invasive and other problematic species, genes & Ongoing Unknown Unknown Unknown diseases -> 8.1. Invasive non-native/alien species/diseases -> 8.1.2. Named species (Parachromis managuensis) Stresses: 2. Species Stresses -> 2.2. Species disturbance 2. Species Stresses -> 2.3. Indirect species effects -> 2.3.2. Competition 8. Invasive and other problematic species, genes & Ongoing Unknown Unknown Unknown diseases -> 8.1. Invasive non-native/alien species/diseases -> 8.1.2. Named species (Oreochromis niloticus) Stresses: 2. Species Stresses -> 2.2. Species disturbance 2. Species Stresses -> 2.3. Indirect species effects -> 2.3.2. Competition 9. Pollution -> 9.1. Domestic & urban waste water -> Ongoing Unknown Unknown Unknown 9.1.1. Sewage Stresses: 1. Ecosystem stresses -> 1.2. Ecosystem degradation 2. Species Stresses -> 2.2. Species disturbance 9. Pollution -> 9.1. Domestic & urban waste water -> Ongoing Unknown Unknown Unknown 9.1.2. Run-off Stresses: 1. Ecosystem stresses -> 1.2. Ecosystem degradation 2. Species Stresses -> 2.2. Species disturbance

Conservation Actions in Place (http://www.iucnredlist.org/technical-documents/classification-schemes)

© The IUCN Red List of Threatened Species: Sardinella tawilis – published in 2018. 9 http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T98836352A98886655.en Conservation Actions in Place In-Place Land/Water Protection and Management

Conservation sites identified: Yes, over part of range

Occur in at least one PA: Yes

In-Place Species Management

Subject to ex-situ conservation: Unknown

Conservation Actions Needed (http://www.iucnredlist.org/technical-documents/classification-schemes)

Conservation Actions Needed 2. Land/water management -> 2.1. Site/area management

3. Species management -> 3.1. Species management -> 3.1.1. Harvest management

Research Needed (http://www.iucnredlist.org/technical-documents/classification-schemes)

Research Needed 2. Conservation Planning -> 2.1. Species Action/Recovery Plan

2. Conservation Planning -> 2.2. Area-based Management Plan

3. Monitoring -> 3.1. Population trends

3. Monitoring -> 3.2. Harvest level trends

Additional Data Fields

Distribution Estimated area of occupancy (AOO) (km²): 244

Estimated extent of occurrence (EOO) (km²): 297

Number of Locations: 1

Lower depth limit (m): 50

Upper depth limit (m): 0

Habitats and Ecology Generation Length (years): 3

Movement patterns: Unknown

Congregatory: Congregatory (and dispersive)

Errata reason: Map was omitted when the assessment was published; errata created to include the map.

© The IUCN Red List of Threatened Species: Sardinella tawilis – published in 2018. 11 http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T98836352A98886655.en The IUCN Red List of Threatened Species™ ISSN 2307-8235 (online) IUCN 2008: T98836352A143839946 Scope: Global Language: English

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The IUCN Red List Partners are: Arizona State University; BirdLife International; Botanic Gardens Conservation International; Conservation International; NatureServe; Royal Botanic Gardens, Kew; Sapienza University of Rome; Texas A&M University; and Zoological Society of London.

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