A re-evaluation of the species limits in Asian white-eyes Zosterops: implications and an appeal for information to assess the status of the newly-recognised Sangkar White-eye Z. melanurus

The complex of white-eyes that are currently recognised as the species Mountain White-eye Zosterops montanus, Japanese White-eye Z. japonicus, Oriental White-eye Z. palpebrosus, Enggano White-eye Z. salvadorii and Everett’s White-eye Z. everetti (del Hoyo et al. 2016) have been comprehensively reassessed following Wells (2017a, b), Round et al. (2017) and Lim et al. (2019). Three new taxa have been recognised.

  • Hume’s White-eye Zosterops auriventer Hume 1878, split from Oriental White-eye along with the parts of Everett’s White-eye away from the Philippines; wetmorei and tahanensis, plus medius (previously included within tahanensis) is elevated to subspecies. Range: central Tenasserim, SE Myanmar, South-central Thailand and south through the Thai-Malay Peninsular and S Myanmar (Tenasserim), and Borneo, (Sabah and locally in C, E and S Kalimantan) (del Hoyo et al. 2016, Wells 2017b).
  • Sangkar White-eye Zosterops melanurus, split from Z. palpebrosus, with subspecies melanurus and buxtoni, but with Sumatran populations of buxtoni tentatively accepted as being a previously misidentified population of Z. auriventer tahanensis, per Lim et al. (2019). Range: Java and Bali.
  • Swinhoe’s White-eye Zosterops simplex, with subspecies simplex, hainanus, erwini (previously part of Z. p. auriventer), williamsoni from Z. palpebrosus, and the previously recognised Enggano White-eye Zosterops salvadorii, now lumped. Range: breeding E China, from Gansu east of Jiangsu, south to Taiwan (China), Hainan, northeast Vietnam, north Laos and northeast Myanmar (present year-round in the southern half of this area) and non-breeding south to Thailand and central Indochina, plus also resident in the Sundaic region (S. Myanmar, S. Thailand from Ranong and Surat Thani, also Ko Samui, peninsular Malaysia, lowland Sumatra and western lowland Borneo) and around the Gulf of Thailand (from Cambodia and south in Thailand to Pattani at least).

One additional taxon has been lumped.

  • Japanese White-eye Zosterops japonicus is lumped into Mountain White-eye Z. japonicus, with the subspecies japonicus, insularis, loochooensis, diatoensis, stejnegeri, alani, montanus, whiteheadi, halconensis, parkesi, pectoralis, diuatiae, volcani (note spelling change), difficilis and obstinatus.

Further subspecies rearrangement has taken place.

  • Ashy-bellied White-eye Zosterops citrinella now includes unicus, previously included within Z. palpebrosus.
  • Following the re-allocation of the subspecies as outlined above, Oriental White-eye is renamed Indian White-eye Zosterops palpebrosus, with subspecies palpebrosus, nilgiriensis, salimalii, egregious, siamensis and nicobarius. New range: SE Arabia, S Iran, NE Afghanistan, Pakistan and India (including Laccadive Is.), Sri Lanka, Andaman and Nicobar Islands (except S), Nepal, and Bhutan, Myanmar (except far SE), SW China, N, E and SE Thailand and NW Indochina.   
  • Everett’s White-eye Zosterops everetti is now restricted to the Philippines and Talaud Islands, Indonesia with the subspecies boholensis, everetti, siquijorensis, basilicanus, mandibularis and babelo.

Most of these newly-defined taxa are unlikely to be listed as threatened on the Red List. However, the status of the newly recognised Sangkar White-eye is suggested to be of considerable concern due to the incredible volume of trade in the species (Eaton et al. 2015, Lim et al. 2019). A brief outline of the assessment for all newly-defined taxa is given below, followed by a full assessment against each criterion for Sangkar White-eye.

Swinhoe’s White-eye Zosterops simplex

The new range of this species as constituted far exceeds the range thresholds for listing as threatened under Criterion B and it is also considered to have a very large population size. It is described as common in most of the range, indeed the most common bird in secondary forest on Hong Kong, but it is also the most popular cagebird in China (van Balen 2019). It is abundant on Taiwan. The subspecies Z. s. williamsoni is considered common around the Gulf of Thailand and Z. s. erwini (the subspecies previously subsumed within Z. palpebrosus auriventer) is common in peninsular Malaysia, but scarce in Malaysian Borneo and Brunei. On Sumatra the species was common, but there are concerns that the very high numbers of individuals trapped may be impacting the population. Subspecies Z. s. salvadorii is abundant in wooded areas on Enggano (Eaton et al. 2016). As such, the species does not qualify for listing as threatened under Criteria B, C or D. No quantitative assessment of the probability of extinction has been conducted for this species, and so it cannot be assessed against Criterion E. Despite very high levels of trapping in parts of the species’s range, it remains abundant in many places. While an overall slow decline may be inferred, it is not believed to approach the thresholds for listing as threatened under Criterion A (at least a 30% decline in 10 years, as in this species three generations is less than 10 years [BirdLife International in prep.]). Consequently, Swinhoe’s White-eye is assessed as Least Concern.

Indian White-eye Zosterops palpebrosus

The newly constituted Z. palpebrosus has a very large range and is assumed to have a very large population size, hence is considered Least Concern

Hume’s White-eye Zosterops auriventer

While the status of the new nominate subspecies of this newly-defined taxon is unclear, the taxon is considered locally fairly common in forest habitat (including plantations) in the Thai-Malay Peninsular but scarce in Sabah (Eaton et al. 2016). There has been considerable forest loss within the range of the species, but the rate of this loss is slower in the upper elevations. For species with lowland Sundaic distributions, rates of loss are up to 1.8% annually (e.g. Cinnamon-headed Fruit-dove Treron fulvicollis: 1.67%, Garnet Pitta Erythropitta granatina: 1.58%). Even using this pessimistic rate (with deforestation encroaching to higher elevations), the rate of decline over the relevant 10 year period does not approach the thresholds for listing as threatened, especially given the species’s tolerance of plantation habitats, but is sufficient to infer a continuing decline in the population. Hence, the species is assessed as Least Concern under Criterion A. The range of the new species is very large, and the population size is thought to exceed the thresholds for listing as threatened. It does not therefore approach the thresholds for listing as threatened under criteria B, C, or D, and Hume’s White-eye is assessed as Least Concern.

Mountain White-eye Zosterops japonicus

This taxon now includes the Japanese White-eye (current BirdLife factsheet), currently listed as Least Concern, and was previously also itself assessed as Least Concern (current BirdLife factsheet). The reconfiguration of the species has not altered the assessment that the species has an extremely large range and is not believed to approach the thresholds for listing as threatened under any of the criteria. Mountain White-eye, as now recognised, is assessed as Least Concern.

Ashy-bellied White-eye Zosterops citrinella

This taxon (BirdLife species factsheet) has seen the addition of the subspecies unicus, which adds the islands of Sumbawa and Flores to the range. Already considered Least Concern, this increases both the range and the global population size of the species, hence Ashy-bellied White-eye continues to be assessed as Least Concern

Everett’s White-eye Zosterops everetti

This newly defined taxon (BirdLife species factsheet) is present in the southern Philippine Islands, including the Sulu Archipelago and on Talaud. It is common throughout its restricted range (Kennedy et al. 2000), and does not approach the thresholds for listing as threatened under Criterion B. Equally, the population is not believed to approach the thresholds for listing under Criteria C or D. Rates of forest loss have greatly slowed in the Philippines. Taking into account this species’s tolerance of plantation and degraded forest, over the past 10 years the rate of decline is not believed to approach the thresholds for listing as threatened under Criterion A. No quantitative assessment of the species’s risk of extinction has been undertaken, so the species cannot be assessed under criterion E. Consequently, Everett’s White-eye is assessed as Least Concern.

Sangkar White-eye Zosterops melanurus

Criterion A – A staggering number of ‘Oriental’ White-eyes are sold in markets on Java, and the vast majority are assumed to be trapped on Java, hence are Sangkar White-eyes Zosterops melanurus. 3,538 individuals were counted for sale in 71 shops in Surabaya, Malang and Yogyakarta between the 22nd and 24th June 2015 (Chng and Eaton2016), while 2,339 individuals were counted in three Jakarta markets (37 shops) between 21st and 23rd July 2015 (Chng et al. 2015). This average of 50 -63 birds per shop is unlikely to be atypical: it really is available in huge numbers on any given day.

In the absence of trapping, the species would likely be one of the commonest birds on Java and Bali: the species does remain ‘common’ (Eaton et al. 2016) and is frequently seen throughout this range (eBird 2019). Yet, there is certainly an impact of this rate of harvest. Lim et al. (2019) suggest that on the basis of the observed numbers in markets, the species should be listed as Vulnerable under Criterion A2d, as a ‘30% reduction in global population size over the past 10 years is a reasonable – if not conservative – assumption’.

Between 1980-1985, van Balen (Diamond et al. 1987) made regular visits to markets around Bogor, and ranked the frequency with which Oriental White-eye (assumed here to equate to Z. melanurus) were offered for sale as ‘occasionally’ on a five-point scale (never, rarely, occasionally, commonly, abundantly). Observations in Bogor in 2014 and 2015 would reclassify this as ‘abundantly’: many hundreds were available in markets close to Bogor Botanical Garden on each of several visits within a 9-month period (R. Martin pers. obs.). This anecdotally suggests that the numbers being supplied have increased, a finding reflected for ‘Oriental White-eye Z. palbebrosus’ observed in Sumatran markets (possibly Z. simplex, possibly imported Z. palbebrosus sensu stricto or a mix of these), where the annual estimate increased fourfold between the early 2000s and 2012 (Harris et al. 2015). The average price (adjusted for inflation) had also increased by nearly 50% in this time, but it remained the third cheapest bird species reported in Harris et al. (2015). It appears that the proxies for identifying overexploitation in a species are being met, and that declines are likely to be occurring at a faster rate within the past three-generation period than in previous decades.

Diamond et al. (1987) found no change in abundance within Bogor Botanical Garden since 1952, and the species continues to occur in apparently similar numbers within this small, well-studied site. The species continued to persist in logged forest and pine plantation to the early 2000s at reasonable density (Sodhi et al. 2005); obviously, a decline could have happened since this study, given the apparent increase in the rate of exploitation.

There appears to be sufficient evidence to infer that there is a continuing decline in the population of the species due to actual levels of exploitation. However, there is no means of quantifying this decline, as local extirpations have not been recorded and no evidence is available from any particular site to show a rate of decline.

To support the assertion that a 30% reduction in the past 10 years is a conservative assumption, there needs to be some evidence of population impact, or a mechanism to estimate the current harvest from the total population size, which is unknown. It is plausible that there has been a decline in excess of 30% in the past 10 years, but the evidence for this is currently lacking. Further information to infer or suspect a decline in excess of 30% within the past 10 years is needed. It is proposed that the species be presently listed as Near Threatened, as it is suspected that it is undergoing a decline that approaches the thresholds for listing as threatened under Criteria A2d+3d+4d.

Criterion B – The Extent of Occurrence (EOO) for the species is 188,758 km2. The species is thus considered Least Concern under Criterion B1.

Criterion C – There is no current population estimate. Due to the rate of trapping it is not possible to estimate a total population from a density estimate. However, the species is still considered ‘common’ (as ‘Sunda White-eye Z, melanurus’, including Sumatra, Borneo and the Lesser Sundas, but explicitly referencing abundance in the range from Sumatra to the Lesser Sundas as common; Eaton et al. 2016), and it occurs from <100 m to 1,600 m on Java (van Balen 1999). Consequently, the population is considered likely to continue to exceed the threshold for listing as threatened under Criterion C, and Sangkar White-eye is assessed as Least Concern under this criterion.    

Criterion D – The population is considered to exceed the thresholds for listing as threatened under Criterion D, hence the species is considered Least Concern under this criterion.

Criterion E – To the best of our knowledge, no quantitative assessment of the probability of extinction has been conducted for this species, and so it cannot be assessed against this criterion.

Based on the above assessment, it is proposed to list Sangkar White-eye (Zosterops melanurus) as Near Threatened, approaching the thresholds for listing as threatened under Criteria A2d+3d+4d. Evidence of extirpations from sites occupied within the relevant period could help to refine the estimate of the suspected rate of decline: any information would be welcome. 

Please note that this topic is not designed to be a general discussion about the ecology of the species, rather a discussion of the species’s Red List status. Therefore, please make sure your comments are about the proposed listing.

*The term ‘location’ refers to a distinct area in which a single threatening event can rapidly affect all individuals of the taxon present, with the size of the location depending on the area covered by the threatening event. Where a taxon is affected by more than one threatening event, location should be defined by considering the most serious plausible threat (IUCN 2001, 2012).

An information booklet on the Red List Categories and Criteria can be downloaded here and the Red List Criteria Summary Sheet can be downloaded here. Detailed guidance on IUCN Red List terms and definitions and the application of the Red List Categories and Criteria can be downloaded here.

References

Chng, S. C. L., Eaton, J. A., Krishnasamy, K., Shepherd, C.R., Nijman, V. (2015) In the Market for Extinction: An inventory of Jakarta’s bird markets. TRAFFIC. Petaling Jaya, Selangor, Malaysia.

Chng, S.C. and Eaton, J.A., 2016. In the market for extinction: eastern and central Java. TRAFFIC Southeast Asia.

Chng, S. C., Guciano, M. & Eaton, J. A. (2016) In the market for extinction: Sukahaji, Bandung, Java, Indonesia. Birding Asia 26: 22-28.

del Hoyo, J., Collar, N. J., Christie, D. A., Elliott, A., Fishpool, L. D. C., Boesman, P. & Kirwan, G. M. (2016) HBW and BirdLife International Illustrated Checklist of the Birds of the World. Volume 2: Passerines. Lynx Edicions and BirdLife International, Barcelona, Spain and Cambridge, UK.

Diamond, J. M., Bishop, K. D. & Balen, S. (1987) Bird Survival in an Isolated Javan Woodland: Island or Mirror? Conservation Biology 1(2): 132-142. doi:10.1111/j.1523-1739.1987.tb00022.x

eBird (2019) eBird: An online database of bird distribution and abundance [web application]. eBird, Ithaca, N.Y., U.S.A. http://www.ebird.org (Accessed on 15/05/2019).

Eaton, J. A., Shepherd, C. R., Rheindt, F. E., Harris, J. B. C., van Balen, S., Wilcove, D. S. & Collar, N. J. (2015) Trade-driven extinctions and near-extinctions of avian taxa in Sundaic Indonesia. Forktail 31: 1-12.

Eaton, J. A., van Balen, S., Brickle, N. W., & Rheindt, F. E. (2016). Birds of the Indonesian Archipelago: Greater Sundas and Wallacea. Lynx Edicions, Barcelona.

Harris, J. B. C., Green, J. M., Prawiradilaga, D. M., Giam, X., Hikmatullah, D., Putra, C. A. & Wilcove, D. S. (2015) Using market data and expert opinion to identify overexploited species in the wild bird trade. Biological Conservation 187: 51-60.

IUCN (2001) IUCN Red List Categories and Criteria: Version 3.1. IUCN Species Survival Commission. IUCN, Gland, Switzerland and Cambridge, U.K.

IUCN (2012) IUCN Red List Categories and Criteria: Version 3.1. Second edition. IUCN Species Survival Commission. IUCN, Gland, Switzerland and Cambridge, U.K. www.iucnredlist.org/technical-documents/categories-and-criteria.

Kennedy, R., Gonzales, P. C., Dickinson, E., Miranda Jr, H. C., & Fisher, T. H. (2000) A guide to the birds of the Philippines. Oxford University Press.

Lim, B. T., Sadanandan, K. R., Dingle, C., Leung, Y. Y., Prawiradilaga, D. M., Irham, M., Ashari, H., Lee, J. G. & Rheindt, F. E. (2019) Molecular evidence suggests radical revision of species limits in the great speciator white-eye genus Zosterops. Journal of Ornithology 160(1): 1-16.

Round, P. D., Manawattana, S., Khudamrongsawat, J., Thunhikorn, S., Safoowong, M. and Bhummakasikara, T. (2017) Disentangling avian diversity: South-East Asian mainland Oriental White-eye Zosterops palpebrosus constitutes two distinct lineages. FORKTAIL 33: 103-115.

Sodhi, N. S., Soh, M. C., Prawiradilaga, D. M. & Brook, B. W. (2005) Persistence of lowland rainforest birds in a recently logged area in central Java. Bird Conservation International 15(2): 173-191.

van Balen, B. (2019) Japanese White-eye (Zosterops japonicus). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (eds.). Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona. (retrieved from https://www.hbw.com/node/60161 on 22 May 2019).

Wells, D.R. (2017a) Zosterops white-eyes in continental South-East Asia. 1: proposed refinements to the regional definition of Oriental White-eye Z. palpebrosusBulletin of the British Ornithologists’ Club 137(2): 100-110.

Wells, D. R. (2017b) Zosterops white-eyes in continental South-East Asia. 2: what is Zosterops auriventer Hume? Bulletin of the British Ornithologists’ Club 137(2): 110-116

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2 Responses to A re-evaluation of the species limits in Asian white-eyes Zosterops: implications and an appeal for information to assess the status of the newly-recognised Sangkar White-eye Z. melanurus

  1. Frank Rheindt says:

    In Lim et al. (2019), we recommended Vulnerable listing for Sangkar White-eye under Criterion A2d, but this recommendation is here ignored because “…there needs to be some evidence of … impact, or a mechanism to estimate the current harvest…”.

    Anecdotal evidence is admitted to allow for the conclusion that “…the species continues to occur in apparently similar numbers…”, but this evidence is taken from Bogor Botanical Garden, a heavily-fenced and unique site where military personnel guard the private residence of the president and where poaching is least likely on Java. If the anecdotal evidence gathered by many colleagues and myself from more conventional Javan sites were to be allowed, a significant population reduction of this species throughout Java would become unequivocal.

    • Rob Martin says:

      Frank, thanks for commenting. The recommendation is not ignored, but the presentation of additional anecdotal information from ‘conventional Javan sites’ is not given in Lim et al. (2019), and is exactly what is needed here to support the conclusion in the paper, such that this assessment is justified.

      Such a summary of observations does not appear to be available in the literature, or at least I cannot find it. Can you and others bring together this information here?

      The species is at least Near Threatened, but this is not necessarily the final category.

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