Research Article |
Corresponding author: Phillip J. Haubrock ( phillip.haubrock@senckenberg.de ) Corresponding author: Darren C. J. Yeo ( dbsyeod@nus.edu.sg ) Academic editor: Franz Essl
© 2021 Phillip J. Haubrock, Ross N. Cuthbert, Darren C. J. Yeo, Achyut Kumar Banerjee, Chunlong Liu, Christophe Diagne, Franck Courchamp.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Haubrock PJ, Cuthbert RN, Yeo DCJ, Banerjee AK, Liu C, Diagne C, Courchamp F (2021) Biological invasions in Singapore and Southeast Asia: data gaps fail to mask potentially massive economic costs. In: Zenni RD, McDermott S, García-Berthou E, Essl F (Eds) The economic costs of biological invasions around the world. NeoBiota 67: 131-152. https://doi.org/10.3897/neobiota.67.64560
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The impacts of invasive alien species are well-known and are categorised as a leading contributor to biodiversity loss globally. However, relatively little is known about the monetary costs incurred from invasions on national economies, hampering management responses. In this study, we used published data to describe the economic cost of invasions in Southeast Asia, with a focus on Singapore – a biodiversity-rich, tropical island city state with small size, high human density and high trade volume, three factors likely to increase invasions. In this country, as well as in others in Southeast Asia, cost data were scarce, with recorded costs available for only a small fraction of the species known to be invasive. Yet, the overall available economic costs to Singapore were estimated to be ~ US$ 1.72 billion in total since 1975 (after accounting for inflation), which is approximately one tenth of the total cost recorded in all of Southeast Asia (US$ 16.9 billion). These costs, in Singapore and Southeast Asia, were mostly linked to insects in the family Culicidae (principally Aedes spp.) and associated with damage, resource loss, healthcare and control-related spending. Projections for 11 additional species known to be invasive in Singapore, but with recorded costs only from abroad, amounted to an additional US$ 893.13 million, showing the potential huge gap between recorded and actual costs (cost records remain missing for over 90% of invasive species). No costs within the database for Singapore – or for other Southeast Asian countries – were exclusively associated with proactive management, highlighting that a shortage of reporting on the costs of invasions is mirrored by a lack of investment in management. Moreover, invasion cost entries in Singapore were under-reported relative to import levels, but total costs exceeded expectations, based on land area and population size, and to a greater extent than in other Southeast Asian countries. Therefore, the evaluation and reporting of economic costs of invasions need to be improved in this region to provide efficient data-based support for mitigation and management of their impacts.
外来物种入侵新加坡和东南亚:数据缺乏不能掩盖潜在巨大的经济损失 众所周知,外来物种入侵的影响是导致全球生物多样性降低的一个重要因素。然而,对于外来物种入侵造成国家经济损失知之甚少,从而阻碍了有效的管理响应。在这项研究中,我们使用已发表的数据揭示外来物种入侵东南亚造成的经济损失,重点关注新加坡:一个生物多样性丰富的热带岛屿城市国家,面积小、人口密度高、进出口贸易量大,这三个因素可能会增加入侵。新加坡和东南亚的其他国家一样缺乏外来物种入侵造成经济损失的数据,只有一小部分已知的入侵物种造成经济损失的记录。然而,自1975年以来,外来物种入侵在新加坡造成经济损失估计约为17.2亿美元(考虑到通货膨胀),约占整个东南亚经济损失(169亿美元)的十分之一。外来物种入侵在新加坡和东南亚的造成的经济损失主要与蚊科(Culicidae)昆虫(主要是伊蚊)有关,与其造成的直接伤害、资源损失、医疗保障和防治的开支有关。根据在其他国家造成损失的经验,估算另外11种在新加坡入侵物种造成了8.9313亿美元的经济损失,这一结果表明记录和实际损失之间的巨大差距(超过90%的入侵物种的缺乏造成经济损失的记录)。在新加坡或其他东南亚国家的数据库中,没有外来入侵物种造成经济损失的记录,因此缺乏前瞻性的管理措施。这突出表明,对于入侵物种造成经济损失报告的短缺与相关管理投资的缺乏是一致的。此外,相对于进口水平,新加坡的入侵物种造成的经济损失是被低估的,根据土地面积和人口规模,总的经济损失超过了预期,远远高于其他东南亚国家。因此,在这个地区需要加强对入侵物种造成经济损失的评估和报告,从而为减轻和管理其影响提供有效的数据支持。
Penaklukan spesis di Singapura dan Asia Tenggara: jurang data gagal untuk menutup kos ekonomi yang berpotensi besar). Kesan buruk spesies asing invasif diketahui ramai dan dikategorikan sebagai penyumbang utama kehilangan biodiversiti di peringkat global. Walau bagaimanapun, tindak balas pengurusan terhalang kerana kekurangan maklumat tentang penilaian kewangan yang timbul daripada penaklukan spesis asing invasif terhadap ekonomi negara. Dalam kajian ini, kami menggunakan data yang telah diterbitkan untuk menggambarkan kos ekonomi penaklukan spesis di Asia Tenggara, dengan fokus pada Singapura – sebuah negara pulau tropika yang kaya dengan biodiversiti, mempunyai saiz kecil, kepadatan manusia yang tinggi dan jumlah perdagangan yang tinggi, tiga faktor yang berkemungkinan meningkatkan penaklukan spesis. Di negara ini, dan juga di negara-negara lain di Asia Tenggara, data kos masih kekurangan, dengan kos yang sedia ada cuma untuk sebilangan kecil spesies yang diketahui invasif. Namun, keseluruhan kos ekonomi yang tersedia untuk Singapura dianggarkan ~ US$ 1.72 bilion secara keseluruhan sejak tahun 1975 (setelah memperhitungkan inflasi), yang merupakan kira-kira sepersepuluh daripada jumlah kos yang dilaporkan di seluruh Asia Tenggara (US$ 16.9 bilion). Kos ini, di Singapura dan Asia Tenggara, kebanyakannya berkaitan dengan serangga dalam keluarga Culicidae (terutamanya, Aedes spp.) dan berkaitan dengan kerosakan, kehilangan sumber daya, penjagaan kesihatan dan perbelanjaan yang berkaitan dengan kawalan. Jangkaan untuk 11 spesies tambahan yang diketahui invasif di Singapura, tetapi hanya dengan menggunakan kos yang dilaporkan dari luar negara, berjumlah US$ 893.13 juta tambahan, menunjukkan potensi adanya jurang besar antara kos yang direkodkan dan yang sebenar (laporan kos masih tiada untuk lebih daripada 90% invasif spesies). Kos dalam pangkalan data untuk Singapura – atau untuk negara-negara Asia Tenggara lain – tidak dikaitkan secara eksklusif dengan pengurusan proaktif. Ini menunjukkan bahawa kekurangan laporan tentang kos penaklukan spesis dicerminkan oleh kekurang pelaburan untuk pengurusan. Lebih-lebih lagi, kemasukan kos penaklukan spesis di Singapura kurang dilaporkan berkaitan dengan tahap import, tetapi jumlah kos melebihi jangkaan, berdasarkan keluasan tanah dan saiz penduduk, dan di tahap yang lebih tinggi daripada negara-negara Asia Tenggara yang lain. Oleh itu, penilaian dan pelaporan kos ekonomi penaklukan spesis perlu ditingkatkan di rantau ini untuk memberikan sokongan berasaskan data yang efisien untuk mengurangkan dan menguruskan kesan buruk akibat spesis asing invasif.
Invasions biologiques à Singapour et en Asie du Sud-Est: les lacunes dans les données ne masquent pas des coûts économiques potentiellement énormes. Les impacts des espèces exotiques envahissantes (EEE) sont bien connus et sont classés comme l’un des principaux contributeurs à la perte de biodiversité à l’échelle mondiale. Cependant, on en sait relativement peu sur les coûts monétaires induits par les invasions sur les économies nationales, qui entravent les décisions de gestion. Dans cette étude, nous avons utilisé des données publiées pour décrire le coût économique des invasions en Asie du Sud-Est, en mettant l’accent sur Singapour - une ville-état insulaire tropicale riche en biodiversité de petite taille, avec une densité humaine et un volume commercial élevés; trois facteurs susceptibles d’augmenter les invasions. Dans ce pays, ainsi que dans d’autres en Asie du Sud-Est, les données sur les coûts étaient rares, les coûts enregistrés n’étant disponibles que pour une petite fraction des espèces réputées envahissantes. Pourtant, les coûts économiques globaux disponibles pour Singapour ont été estimés à au moins ~ 1,72 milliard de dollars américains, soit environ un dixième du coût total enregistré dans toute l’Asie du Sud-Est (16,9 milliards de dollars américains). Ces coûts, à Singapour et en Asie du Sud-Est, étaient principalement liés aux insectes de la famille des Culicidae (principalement Aedes spp.) et associés aux dommages, à la perte de ressources, aux soins de santé et aux dépenses liées au contrôle. Les projections pour 11 espèces supplémentaires connues pour être envahissantes à Singapour, mais avec des coûts enregistrés uniquement en provenance de l’étranger, se sont élevées à 893,13 millions USD supplémentaires, montrant l’énorme écart potentiel entre les coûts enregistrés et réels (les enregistrements de coûts restent manquants pour plus de 90% des espèces envahissantes). Aucun coût dans la base de données pour Singapour - ou pour d’autres pays d’Asie du Sud-Est - n’était exclusivement associé à une gestion proactive, ce qui souligne qu’un manque de rapports sur les coûts des invasions se traduit par un manque d’investissement dans la gestion. De plus, les entrées de coûts d’invasion à Singapour ont été sous-déclarées par rapport aux niveaux d’importation, mais les coûts totaux ont dépassé les attentes fondées sur la superficie des terres et la taille de la population, et dans une plus grande mesure que dans d’autres pays d’Asie du Sud-Est. Par conséquent, l’évaluation et la communication des coûts économiques des invasions doivent être améliorées dans cette région pour fournir un soutien efficace basé sur des données pour l’atténuation et la gestion de leurs impacts.
Invasiones biológicas en Singapur y el sudeste asiático: la falta de datos no logra enmascarar costos económicos potencialmente masivos. Los impactos de las especies invasoras son bien conocidos y se caracterizan por ser uno de los principales contribuyentes para la pérdida de la biodiversidad a nivel global. No obstante, se conoce relativamente poco sobre el impacto monetario que las invasiones provocan en las economías de las naciones, lo cual obstaculiza las respuestas de manejo. En el presente estudio, se emplearon datos publicados para describir los costes económicos de las especies invasoras en el sudeste asiático, con un enfoque en Singapur –una pequeña ciudad isleña tropical con alta riqueza biológica, alta densidad poblacional y un alto volumen del mercado; tres factores que se asocian con el incremento de invasiones biológicas–. En este país, como en otros del sudeste de Asia, los datos sobre los costes son escasos, donde los registros de costes disponibles representaron solo una fracción de las especies que se conocen como invasoras. No obstante, los datos sobre los costes económicos disponibles en general se estimaron al menos en ~ US $1.72 mil millones en Singapur, lo cual corresponde aproximadamente a una onceava parte de los costes reportados en todo el sudeste de Asia (US $16.9 mil millones). Los costes identificados en Singapur y el sudeste asiático se asociaron principalmente con insectos de la familia Culicidae (principalmente Aedes spp.) y se asociaron con gastos por daños, pérdida de recursos, cuidado de la salud, y aquellos relacionados con el control. Las proyecciones para las 11 especies adicionales que se sabe que son invasoras en Singapur, pero con registros superficiales en sus costes, alcanzaron un total de US $893.13 millones, mostrando un gran vacío potencial entre la información registrada y los costes actuales (los registros mantienen una ausencia sobre los costes del 90% de las especies invasoras). Ningún coste en la base de datos de Singapur –o para otro país sudasiático– se asoció exclusivamente con manejo proactivo, destacando que la escasez de información sobre los costes de las invasiones se refleja en la falta de inversión en el manejo. Además, las entradas de los costes de invasoras se mostraron inferiores a los niveles de importación en Singapur, pero los costes totales superaron las expectativas basadas en la extensión del área y el tamaño de la población, y en mayor medida que en otros países del sudeste de Asia. Por lo tanto, es necesario mejorar la evaluación y la presentación de informes sobre los costes económicos de las invasiones en esta región a fin de proporcionar un apoyo eficaz basado en datos para la mitigación y el manejo de sus impactos.
Ecosystem services, imports, InvaCost, monetary impact, tropics, socioeconomic sectors
Biological invasions cause significant ecological impacts around the world, posing profound impediments to conservation efforts and potentially driving marked socioeconomic costs (
Whilst the ecological impacts of invasive species are well-described (see, for example,
As an international travel and trade hub with numerous introduction pathways, Singapore is a country facing high risk of biological invasions (
Recently, the available literature on economic costs of invasive species globally was compiled in the InvaCost database (Diagne et al. 2020b) with the aim of generating the means to fill knowledge gaps on invasion costs worldwide. Using data available from this database, we synthesised and described the available information on economic costs of invasions in Southeast Asia, focusing on Singapore in particular. We specifically investigated (a) how recorded costs and species are characterised across Southeast Asian countries and (b) Singapore as a more detailed example or case study to describe recorded costs impacting its economy, according to (i) taxa, (ii) cost types and (iii) activity sectors. We also deciphered whether the level of reliability of estimates may impact the financial burden of invaders. Furthermore, we extrapolated additional costs for invaders reported in Singapore, but with unknown costs there. Finally, we correlated invasion costs with importation levels, surface area and population size amongst countries to assess the specificities of Southeast Asian countries. We hypothesised that the costs of invasive species in Singapore are underestimated and yet substantial, as are probably those of other Southeast Asian countries.
Information on the economic cost of invasions in all the Southeast Asian countries (Brunei, Cambodia, East Timor, Indonesia, Laos, Malaysia, Myanmar, Philippine, Singapore, Thailand and Vietnam) was extracted from the InvaCost database (Diagne et al. 2020b;
We considered the total costs of invasions by amalgamating the recorded raw costs (column ‘Cost_estimate_per_year_2017_USD_exchange_rate’) per year from our subset. Due to the variability of temporal scales of cost estimates in InvaCost, we annualised the data, based on the difference between the “Probable_starting_year_adjusted” and “Probable_starting_year_adjusted” columns using the "summarizeCosts" function of the ‘invacost’ package (v.0.3-4) in R (v.4.0.2) (Leroy et al. 2020). Each expanded entry thus corresponded to a single year for which costs were available following this expansion process (i.e. costs spanning multiple years were divided amongst those same years). The resulting costs attributed to recorded species were examined according to different descriptive fields of the database (an updated description of these descriptive fields is openly available at https://doi.org/10.6084/m9.figshare.12668570):
To investigate the temporal dynamics of invasion costs, we used the "summarizeCosts" function implemented in the R package ‘invacost’ (Leroy et al. 2020). With this method, we calculated the observed cumulative and average annual costs covering the period for which costs were recorded, displaying the changes in invasion costs over time.
As cost information for invasive alien species in Singapore, which we used as an example, was limited (three species; see Results for more details), we also extrapolated potential costs for a few additional known invasive species present in Singapore, but which had recorded costs outside Singapore. For this, we used the most recent comprehensive list of alien animal species in Singapore (n = 142;
Given Singapore is an economic centre, we compared the available cost information of Singapore – in terms of cost entries and number of recorded species (
Finally, we examined the relationships between invasion costs (observed and high reliability costs only) and (i) land area and (ii) human population size using linear regressions (log-transformed) and examined how Singapore compared to other countries globally and in Southeast Asia particularly. Land area and population size per country were obtained using 2020 data from worldometer (https://www.worldometers.info/world-population/population-by-country/).
Cost data originated from seven records from six different published sources (n = 34 expanded entries). The recorded costs were found to have occurred after 1975 and amounted to US$ 1.720 billion in total (Figure
Relative proportions of known alien species present and recorded costs in Singapore as of 2010 (
At the taxonomic level, cost estimates were available for species from two families, Culicidae (n = 6 estimates) and Corvidae (n = 1). Within Culicidae, Aedes spp. drove all of the recorded costs, with four records attributed to A. aegypti alone and two as a combination of A. aegypti and A. albopictus. Although A. albopictus is native to Singapore, it was not possible to separate joint cost estimates, which accounted for < 0.05% of total Culicidae costs. For Corvidae, the single cost estimate was associated with Corvus splendens.
The overall estimated cost was mainly caused by Aedes spp. with a total of US$ 1.72 billion split between damage-losses (US$ 1.14 billion) and management costs (US$ 578.01 million). For C. splendens, the single cost estimate reached US$ 765.24 thousand and concerned costs attributed to control-related management efforts (Figure
From a methodological point of view, all reported costs were classified as “Observed”, i.e. considered as actually occurring and not based on predictions or extrapolations from outside the invaded area. Every documented Aedes spp. cost was obtained from accessible peer-reviewed literature and thus deemed “High reliability”. Conversely, the single cost estimate of C. splendens was deemed to be of “Low reliability” (Figure
Costs for invasive species were recorded between 1975 and 2014. These costs tended to increase over time, both in terms of reported costs (1975–1994: n = 2; 1995–2014: n = 32), but also average annual costs (1975–1994: US$ 1.66 million per year; 1995–2014: US$ 80.24 million per year), with an annual average cost total of US$ 41.91 million across the entire period (Suppl. material
Comparing the costs of recorded species in Singapore with their average annual costs per country outside of Singapore, after excluding extreme values (removing 25% extreme values, i.e. the top and bottom 12.5%), costs and expenditure in Singapore were around three times lower than those in the rest of the world. From the 142 species recorded in
The monetary impact of invasions recorded in Southeast Asia totalled US$ 16.89 billion between 1960 and 2020. Amongst these, Singapore ranked fifth relative to other countries in terms of reported costs, with two recorded invasive alien species and seven recorded cost entries in InvaCost. Notably, Brunei had the lowest number of recorded entries (1), species (1) and costs (US$ 6.7 million), while Thailand had the highest costs (US$ 5.2 billion) and most recorded entries (13) according to InvaCost (Table
Comparison of recorded invasive alien species and their costs amongst countries in Southeast Asia. Proportions of species with reported costs, relative to numbers of known reported alien species originating from the Global Alien Species First Records Database (Seebens et al. 2018; accessed in June 2020), are also displayed.
Southeast Asian country | Recorded species | Database entries | Total cost in US$ billion (2017 value) | Species reported | Proportion of recorded established alien species |
---|---|---|---|---|---|
Brunei | 1 (Aedes aegypti) | 1 | 0.007 | - | - |
Cambodia | 1 (Aedes aegypti) | 7 | 0.208 | 10 | 10% |
East Timor | 1 (Aedes aegypti) | 1 | 0.004 | ||
Indonesia | 2 (Aedes aegypti; Rattus sp.) | 5 | 3.406 | 75 | 2.7% |
Laos | 1 (Aedes aegypti) | 1 | 0.054 | 10 | 10% |
Malaysia | 4 (Aedes aegypti; Aedes albopictus, Mus musculus, Rattus norvegicus) | 10 | 2.673 | 36 | 5.6% |
Myanmar | 3 (Aedes aegypti, Mus musculus, Rattus norvegicus) | 3 | 0.152 | 15 | 6.7% |
Philippines | 3 (Aedes aegypti; Pomacea canaliculata; Sternochetus frigidus) | 10 | 3.169 | 70 | 4.3% |
Singapore | 3 (Aedes aegypti; Aedes albopictus; Corvus splendens) | 7 | 1.718 | 142 | 2.6% |
Thailand | 4 (Aedes aegypti; Aedes albopictus, Mus musculus, Rattus norvegicus) | 13 | 5.176 | 45 | 4.4% |
Vietnam | 1 (Aedes aegypti) | 6 | 0.327 | 20 | 5% |
We further identified a significant correlation between trade volume and the number of recorded entries in InvaCost (Suppl. material
Considering all countries, invasion costs related significantly positively to both land area and population size (Supplement 5). When compared to other countries with costs, Singapore displayed considerably greater costs relative to those variables, even relative to other Southeast Asian nations which mostly clustered together (Figures
Relationship between the import value and the number of records in InvaCost, focusing on the 50 countries ranking highest in both GDP and import values, but with recorded data in InvaCost. Note that all variables are displayed on a ln-scale. Singapore shows a large deficit of records related to expectations from its import value.
The recorded invasion costs in Singapore over the past 40 years have reached US$ 1.72 billion in total which represents about ⁵⁄₆ of the Ministry of the Environment and Water Resources (S$ 2.83 billion; US$ 2.12 billion), ⅔ of the Ministry of Trade and Industry (S$ 3.68 billion; US$ 2.76 billion) or more than ⅓ of the Ministry of National Developments (S$ 4.8 billion; US$ 3.67 billion) annual budgets in 2017 (https://www.singaporebudget.gov.sg). Despite these costs being high, our study shows that the available entries in the database were highly fragmentary, with the majority of documented alien animal species in Singapore being absent from the cost estimation (
The very few recorded costs were linked principally to the human health sector and mainly driven by mosquitoes, with large incurred costs listed for healthcare and their control. This is mostly related to costs arising from limiting the risk of infectious human diseases, such as Zika, dengue or chikungunya, which are caused by pathogens, vectored principally by A. aegypti and A. albopictus, as well as losses through direct healthcare costs (Beltrame et al. 2007; Zammarchi et al. 2015). Indeed, mosquitoes are considered as a severe problem in Singapore, underlined by the considerable costs on control and the medical field (Carrasco et al. 2011). These total costs relating to human health in Singapore are significant, considering previous estimation of annual costs on human health and environment in the entirety of Southeast Asia (US$ 1.85 billion; US$ 1.4–2.5 billion per year) estimated by
In the context of Southeast Asia, this national bias is even more pronounced; amidst differences in economic activities amongst countries (note that Singapore has the highest GDP per capita in Southeast Asia), the lack of cost information for invasive alien species more broadly across Southeast Asian countries is striking. Singapore had the lowest proportion of known invasive alien species with reported costs, while all Southeast Asian countries had costs for 10% or below in terms of listed invasive alien species. This is also noteworthy in an all-Asia context (
Regarding the overall cost estimation, it is possible to overestimate costs if one assumes that the costs repeatedly occurring over time are repeated for a longer duration than it actually occurs (if total duration is not reported). To stay conservative, we assigned a single duration year for cost entries for which such information was missing and the cost was potentially ongoing. Furthermore, it is possible that the annual monetary burden increased over the years due to frequent descriptions of new invaders. In addition, the spatial scale for estimating costs in InvaCost reflect ‘site’ and/or ‘country’ level estimates, meaning that the national burden could be higher as some ‘regional’ costs may not have specified specific countries. Additionally, we show that the relatively large number of alien species present in Singapore (see
Our work also reveals a considerable taxonomic bias in the reported economic impacts of the 142 reported alien animal species in Singapore. The weighting of costs towards taxa in the database does not reflect the ‘true’ taxonomic composition of alien species in Singapore. Freshwater fishes and reptiles together make up the majority of alien species in this country (61%) (
Whilst we cannot exclude that some existing cost data may have not been captured by the InvaCost database, this taxonomic discrepancy should be discussed. Singapore has a history of freshwater species introductions (
Given that management and control costs usually outweigh the costs of prevention and surveillance (
Despite most of the economic costs in Singapore being related to the control of invasive species and the costs of healthcare, it can be assumed that other damage or losses have not yet been estimated. For example, similarly data-poor studies found major costs for agriculture in Argentina or the UK (
The authors acknowledge the French National Research Agency (ANR-14-CE02-0021) and the BNP-Paribas Foundation Climate Initiative for funding the InvaCost project that allowed the construction of the InvaCost database. The present work was conducted following a workshop funded by the AXA Research Fund Chair of Invasion Biology and is part of the AlienScenario project funded by BiodivERsA and Belmont-Forum call 2018 on biodiversity scenarios. RNC is funded by a research fellowship from the Alexander von Humboldt foundation. CD is funded by the BiodivERsA-Belmont Forum Project “Alien Scenarios” (BMBF/PT DLR 01LC1807C). The authors also acknowledge the constructive and helpful comments of the anonymous reviewers. Further, the authors acknowledge Wen Xiong, Axel E. Rico-Sanchez and Anna Turbelin for the translation of abstracts.
Description of the procedure used for collecting and describing cost data in the InvaCost database (adapted from Diagne et al. 2020)
Data type: database description
Database subset
Data type: database
Annual average costs of biological invasions in Singapore. Note the y-axis is on a log10 scale
Data type: database
Extrapolated annual average costs for those invasive species known to be in Singapore with recorded costs in InvaCost
Data type: database
Relationships between trade value and recorded cost entries per country in InvaCost, as well as land area and human population with total cost
Data type: database