A modelling implementation of climate change on biodegradation of Low-Density Polyethylene (LDPE) by Aspergillus niger in soil Academic research paper on "Biological sciences"

Contents lists available at ScienceDirect

Global Ecology and Conservation

journal homepage: www.elsevier.com/locate/gecco

Original research article

A modelling implementation of climate change on biodégradation of Low-Density Polyethylene (LDPE) by Aspergillus niger in soil

CrossMaik

Farzin Shabania'*, Lalit Kumara, Atefeh Esmaeili

a Ecosystem Management, School of Environmental and Rural Science, University of New England, Armidale, NSW, 2351, Australia b Soil Science Department, Faculty of Agricultural Engineering and Technology, University College of Agriculture and Natural Resources, University ofTehran, Tehran, Iran

article info

Article history:

Received 25 April 2015

Received in revised form 4 August 2015

Accepted 15 August 2015

Keywords:

Microbial degradation Aspergillus niger Polyethylene CLIMEX Climate change

abstract

Aim: To model the areas becoming and remaining highly suitable for Aspergillus niger growth over the next ninety years by future climate alteration, in relation to the species' potential enhancement of Low Density Polyethylene (LDPE) biodegradation in soil. Location: Global scale

Methods: Projections of A. niger growth suitability for 2030, 2050, 2070 and 2100 were made using the A2 emissions scenario together with two Global Climate Models (GCMs): the CSIR0-Mk3.0 (CS) model and the MIROC-H (MR) model through CLIMEX software. Subsequently the outputs of the two GCMs were overlaid to extract common areas in each period of time, providing higher certainty concerning areas which will become highly suitable to A. niger in the future. Afterwards, GIS software was employed to extract sustainable regions for this species growth from present time up to 2100.

Results: Central and eastern Argentina, Uruguay, southern Brazil, eastern United States, southern France, northern Spain, central and southern Italy, southern Hungary, eastern Albania, south western Russia, central and eastern China, eastern Australia, south east of South Africa, central Zambia, Rwanda, Burundi, central Kenya, central Ethiopia and north eastern Oman will be highly suitable for A. niger growth from present time up to 2100. Main conclusions: Accurately evaluating the impact of landfilling on land use and predicting future climate are vital components for effective long-term planning of waste management. From a social and economic perspective, utilization of our mapped projections to detect suitable regions for establishing landfills in areas highly sustainable for microorganisms like A. niger growth will allow a significant cost reduction and improve the performance of biodegradation of LDPE over a long period of time, through making use of natural climatic and environmental factors.

© 2015 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Plastics are chemically synthesized long-chain polymers (Scott, 1999) and are globally produced on a substantial scale. The major characteristics of plastic are its strength yet lightness, flexibility, moisture resistance, versatility and its relatively

* Corresponding author.

E-mail address: fshaban2@une.edu.au (F. Shabani).

http://dx.doi.Org/10.1016/j.gecco.2015.08.003

2351-9894/© 2015 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).

low cost (Reddy et al., 2014). Such characteristics explain the enormous worldwide consumption of this material. However, the durability of plastic materials means they are slow to degrade and thus a further characteristic is their staying power as a waste. Thus, the enormous human usage of plastics, together with undeniably negative behaviour related to excessive consumption, thoughtless discarding and littering and consequently polluting, is a lethal combination.

The accumulation and slow degradation of plastics has in recent years produced ubiquitous and long-lasting changes affecting the surface of our planet. Plastic debris affects wildlife and human habitat and is thus a major concern internationally (Sheavly and Register, 2007). Plastic debris may hamper the mobility of animals, prevent eating, cause cuts and wounds, suffocation and even drowning. Fishing ropes, nets and monofilament lines, balloons, rings of six-packs, and packaging straps are among the harmful products causing entanglements. The US Marine Mammal Commission reports the involvement in entanglements of 136 marine species, including six sea turtle species, 51 seabird species, and 32 marine mammal species (Commission, 1998). It has also been documented that plastics weighing more than 40 million tons are produced annually and discarded into the environment (Yang et al., 2007). Based on a recent estimate of the Central Pollution Control Board, New Delhi, India, 8 million tons of plastic products are consumed every year in India. A study on plastic waste production in 60 major Indian cities revealed that roughly 15,500 tons of plastic waste is generated daily by the nation (Central Pollution Control Board in New Delhi in India, 2013). It should be noted that Low-density polyethylene (mainly used as carry bags) constitutes the major portion of this waste problem (Harshvardhan and Jha, 2013).

Landfilling, incineration, recycling, composting and biodegradation are the principal methods of municipal solid waste (MSW) disposal worldwide (Alavi Moghadam et al., 2009). Other than biodegradation, these methods all have disadvantages. In terms of management, disposal of solid waste are the lowest in priority (Bai and Sutanto, 2002; Finnveden et al., 2005; Lazarevic et al., 2010) as plastic waste degradation in the soil over 100 years is only 1%-5%, which leads to the possibility of groundwater and air pollution (Rebeiz and Craft, 1995). Additionally, landfills occupy space, itself a problem on our overcrowded planet (Dijkgraaf and Vollebergh, 2004). Incineration can reduce the final disposal waste volume, simultaneously producing alternative sources of energy in the forms of electricity and/or heat. However, compared with landfills, even with leakage prevention, incineration is too expensive. Incineration itself leads to air emissions, such as carbon dioxide, nitric oxide, nitrogen dioxide and sulphur dioxide, and chemical residuals, such as volatile organic compounds, polycyclic aromatic hydrocarbons, polychlorinated dibenzofurans, dioxins, carcinogenic substances (Dijkgraaf and Vollebergh, 2004; Al-Salem et al., 2009). A related Netherlands study (Lazarevic et al., 2010) showed comparative gross environmental cost per tonne of waste are €46 for incineration and €26 for landfill. The significant reduction of solid waste volume by incineration is offset by the fact that fly ash and bottom ash, the two types of ash produced by incineration, themselves need to be disposed, which leads to the possibility of groundwater and soil pollution by leachate bearing lead, cadmium and other heavy metals (Bai and Sutanto, 2002; Lazarevic et al., 2010). Although recycling has a higher priority than incineration (Finnveden et al., 2005), however, for the complete and effective conversion of plastic waste into useable products there are a number of technological and cost related limiting factors. Plastics, unlike other waste materials, such as paper and aluminium, are not homogeneous, and may consist of a number of grades with variance of molecular structure and property. Plastic generally has low density and therefore, materials are compacted or ground before being transported to reduce costs (Rebeiz and Craft, 1995). If not adequately sorted they maybe contaminated with dirt and metals, damaging the reprocessing equipment. Thus, recycling of plastic materials needs flexibility to cope with a variety of composition, a proper infrastructure for the collection and sorting of waste, constructive technology economically viable for conversion to new products and structures to establish and supply marketability. As a rule, western countries are able to compost successfully but there are a number of reasons why this method is rarely used in other countries: (1) Few residents sort urban solid wastes as sorting equipment needs a financial outlay (2) The majority of users have a traditional resistance to the products derived from waste materials and overall acceptance of composting is low and (3) The usefulness of compost is limited. Further compost can only be used for cultivating non-edible produce, which is a serious economic constraint. Regulations, monitoring and quality control preventing secondary pollution of compost are inadequate (Hui et al., 2006). Furthermore, compost output quality and its application potential is dependent on its heavy metal concentrations, which in turn are dependent on the original quality of raw materials composted (Magrinho et al., 2006). Thus, composting is not currently a highly recommendable recycling method.

The worldwide explosion of plastic waste materials, reduced availability of sites for landfill, and the lack of universal procedures for the safe disposal of plastic waste materials has given rise to considerable researcher interest in identifying methods that can decrease the quantities of plastic waste (Esmaeili et al., 2014). Biodegradation by microorganisms appears to be a potential improvement on landfill disposal, incineration or recycling of plastic waste, all of which have elements of negative environmental and economic constraints, as discussed above (Kapri et al., 2010; Zahra et al., 2010). Biodegradation is a term used to describe the process by which living organisms break down organic substances. Bacteria and fungi have been involved in both natural and synthetic plastics degradation (Shah et al., 2008). Recently, plastic waste and polymer biodegradation has been acknowledged as a potential safer method due to the inefficiency of physical and chemical disposal methods and the consequent environmental damage they cause (Bhalerao and Puranik, 2007; Esmaeili et al., 2013). This method requires the presence of light and air to allow decomposition, as well as the necessary nutrients and sufficient moisture to sustain microbial action (Rebeiz and Craft, 1995). Also, it should be noted that exploiting degrading microorganisms in natural medium such as soil along with abiotic degradation, in order for plastics to become more hydrophilic, would be an environmentally friendly and safe approach, leading to the formation of CO2, water and new biomass as degradation end products.

Synthetic polymers are hydrophobic and thus under normal circumstances are not biodegradable due to their higher molecular mass and their absence of functional groups. However, when degraded to a lower molecular mass through oxidation they can then be assimilated by microorganisms, which means that abiotic degradation in which they are transformed into monomeric and oligomeric products must precede biodegradation (Jakubowicz et al., 2006, 2011). Thus, the degrading of synthetic plastics is an extremely slow process, initially involving environmental factors and thereafter microorganisms (Abd El-Rehim et al., 2004). Physical forces such as heat, sunlight, moisture and pressure initially impact to mechanically damage polymers, followed by the biological action of enzymes and other microbial metabolites acting as catalysts (Nanda et al., 2010). In light of the fact that the metabolic pathways of microorganisms coupled with physical environmental factors such as temperature or moisture are the key elements indispensable for biodegradation (Grima et al., 2000; Abd El-Rehim et al., 2004), some recent plastics have been designed as biodegradable, facilitating the two stage physical and metabolic breakdown (Bonhomme et al., 2003; Yang et al., 2007; Song et al., 2009; O'Brine and Thompson, 2010; Esmaeili et al.,2014).

Recent research (Esmaeili et al., 2013, 2014), has evaluated pure Low-Density Polyethylene (LDPE) films biodegradation without pre-treatment by photo-oxidation or the addition of pro-oxidants in soil with and without mixed cultures of the landfill-source microorganisms, A. niger designated strain F1 and Lysinibacillus xylanilyticus XDB9 (T) designated strain S7-10F. Measurements of the respiration and microbial population data have demonstrated notable differences between the inoculated and un-inoculated treatments. Carbon dioxide levels after 126 days indicated slow biodegradation in the uninoculated treatments with approximately 8.6% and 7.6% mineralization in the UV and non-UV-irradiated LDPE respectively (Esmaeili et al., 2013). The biodegradation showed greater efficiency in the presence of the selected microorganisms, the percentages of biodegradation being 15.8% and 29.5% for non-UVand UV-irradiated films, respectively. It is expected that soon, these microorganisms will be able to be used to reduce solid waste quantities rapidly accumulating in our natural environment.

Aspergillus niger is a cosmopolitan fungus and a well-known species of the genus Aspergillus (Sharma, 2012). It is broadly distributed and has been detected in a broad range of habitats because it can colonize a wide variety of substrates (Mateescu et al., 2011; Sharma, 2012). A. niger is usually found as a saprophyte growing on compost piles, stored grain, dead leaves and other decaying flora. The spores are widespread and associated with organic materials and soil (Sharma, 2012). Many asexual spores produced within the conidiophores are resistant to environmental stresses, which assists the organism to survive during inactive periods. This organism is a soil saprobe with a wide array of hydrolytic and oxidative enzymes involved in the breakdown of plant lignocelluloses. This feature, along with its ability to produce extracellular organic acids, enables it to cause decay of various organic substances (Gautam et al., 2010; Sharma, 2012; Ardestani and Kasebkar, 2014). On the other hand, this fungus is causing food spoilage and bio-deterioration of other materials (Gautam et al., 2010). A. niger also plays an important role in the global carbon cycle (Sharma, 2012). It should be mentioned that Aspergillus species are greatly aerobic and are found in almost all oxygen-rich environments, where they commonly grow as moulds on the surface of a substrate, due to high oxygen tension (Chehri, 2013). Climatic parameters such as humidity and temperature are extremely important in dispersing fungi spores in air for short and long distances and when spores are deposited on a solid or liquid surface and if conditions of moisture and food are appropriate, they germinate. A few researches on airborne fungi reported that an increase in fungi spore concentration was seen at air temperatures between 15 and 25 °C and relative humidity at 60%-70% (Ababutain, 2013).

There has been worldwide research on the potential of climate change impact on different species (Adams et al., 1998). Studies have considered this impact on the production of maize (Jones and Thornton, 2003), cotton (Gossypium) (Reddy et al., 1997; Rogers et al., 2007; Shabani and Kotey, 2015), Fusarium oxysporum f. spp. (Shabani et al., 2014a), wheat (Ortiz et al., 2008), date palm (Shabani et al., 2012, 2014c), Rhynchospora alba (white-beaked sedge) and Salix herbacea (dwarf willow) (Pearson et al., 2002) and Triadica sebifera (Pattison and Mack, 2008). However, to the best of our knowledge, there have been no previous studies on climatic change impact on projected distributions of Aspergillus niger and its potential use in soil in the biodegradation of LDPE.

To make a strategic plan of LDPE waste controlling through biodegradation method, in this study an attempt was made to model the areas becoming and remaining highly suitable for A. niger growth over the next ninety years (2030,2050,2070 and 2100) by future climate alteration using the A2 emissions scenario together with two global climate models (GCMs): the CS1R0-Mk3.0 (CS) and the MIROC-H (MR) using CLIMEX software. Subsequently the outputs of the two GCMs were overlaid to illustrate common areas to both GCMs in each time period, providing higher certainty concerning areas which will become highly suitable to A. niger in the future, and so identifying potential areas where biodegradation could be a viable method of waste management. The model outputs identify those regions that are currently suitable and remain suitable into the future for sustainable A. niger growth.

2. Methodology

2.1. Scenario of climate change, meteorological database and global climate change models (GCMs)

The A1, A2, B1 and B2 scenarios project global-average surface temperatures to rise by 1.4-5.8 °C by the year 2100 (1PCC, 2001). However, these scenarios incorporate differences in their inherent predicted socioeconomic growth and technological

developments. In the case of the A1B scenario, there is a predicated increase of 2.9 °C in global average temperature by 2100. The A1 series incorporates very rapid economic growth, with a mid-century peaking in global population and the development of technologies of greater efficiency. Three scenarios in the series—A1B, A1FI and A1T show differences on the basis of the issue of energy in relation to technological change (IPCC, 2007). A1B assumes a balance between fossil and non-fossil energy technologies, whereas the other two show opposing extremes in the degrees of fossil fuels versus nonfossil fuels. The SRES emission scenario A2 formed the basis of the study as it assumes neither very high nor low global GHG emissions compared to other scenarios such as A1F1, A1B, B2, A1T and B1.

Parameters of climate incorporated in the meteorological database are the mean monthly temperature maximums and minimums (Tmax and Tmjn), precipitation levels (Ptotal) and relative humidity levels, taken at 09H00 (RH09:00) and 15H00 (RH 15:00). These parameters were also used for projecting potential future climates.

From a total of 23 global climate models used to simulate climates of 20th and 21st centuries, we used the well-known GCMs namely: CSIR0Mk3.0 and MIROC-H, in conjunction with the A2 Special Report on Emissions Scenarios (SRES) scenario, for modelling the potential Aspergillus niger future distributions. This scenario was chosen on the basis of its incorporation of the economic, technological and demographic factors impacting on global greenhouse gas (GHG) emissions (IPCC, 2007).

2.2. CLIMEX as a mechanistic niche model

Our research used CLIMEX to model present and future distributions of A. niger. CLIMEX software supports ecological research incorporating the modelling of potential species' distributions under different climate scenarios, and makes the assumption that climate is the paramount determining factor of plant and poikilothermal animal distributions (Kriticos et al., 2007). CLIMEX enables users to determine geographically relevant climatic parameters describing the responses of an organism to climate (Sutherst et al., 2007b). Thus, it models the mechanisms of a species that impose the limitations of its geographical distribution and determines its seasonal phenology and abundance (Sutherst et al., 2007a). Species growth potential in the favourable season is denoted by the Annual Growth Index (GIA), while the impact of population reduction during an unfavourable season is established by the dry, wet, hot, and cold stress indices and the interactions of these parameters (Sutherst et al., 2007a). The Ecoclimatic Index (EI), the product of the GIA and stress indices, rates the level of suitability for species' occupation of a particular location or year. The EI is thus an annual average index, derived from weekly data of the growth and stress indices of the suitability levels of climatic factors, denoted by a value on the scale 0 to 100. A species may be established where EI > 0 (Shabani et al., 2013, 2014a,b, 2015).

2.3. Current distribution of A. niger

Indigenous and alien distributions of A. niger were drawn from literature and other sources such as the Global Biodiversity Information Facility (GBIF), to construct the model (Hang et al., 1975; Hiort et al., 2005; Pappas et al., 2010; Mwanza, 2011). In this study 111 records of A. niger were obtained from literature searches and 15 records from the GBIF database, which were used to fit parameters in CLIMEX. Fig. 1 illustrates the distribution of A. niger on the global scale.

2.4. Fitting CLIMEX parameters

For model framing, parameters of stress were fitted according to the global distribution data, iteratively adjusted to achieve satisfactory agreement between known and projected species' distributions globally. The fitted parameters and results were rechecked to make certain that they were biologically reasonable. The data from the United States was set aside for model validation.

• Wet stress

One of the most important parameters for fungus growth is humidity and it has been documented that the relative humidity for 58 fungi species ranges from 70% to 98%. Of the relative humidity regimes tested in the study of Shehu and Bello (2011), 85% and 100% were the most favourable for the growth of Aspergillus species (Shehu and Bello, 2011). Similarly, Oladiran and Iwu (1993) reported a relative humidity range of 70%-90% to be optimal condition for the growth of A. niger and A.flavus. The optimum relative humidity for A. niger growth is near to 93% (Bonner, 1948). However, it does not necessarily mean that the optimum humidity is at saturation. Two parameters, wet stress threshold (SMWS) and wet stress rate (HWS), account for wet stress in CLIMEX. Wet Stress accumulates if moisture level of the soil exceeds the SMWS. In order to calculate Wet Stress, the difference between soil moisture level (SM) and SMWS is multiplied by HWS. For the purposes of our study, the SMWS and HWS were established at 1.5 and 0.7 respectively, in order to allow good growth of the species in southern Brazil, Spain, United Kingdom, Ukraine and Turkey where they are currently found.

• Heat stress (HS)

In CLIMEX model, Heat Stress has two parameters: the Heat Stress Temperature Threshold (TTHS) represents the high temperature level at which the species can no longer survive and Heat stress rate (THHS) is the rate at which stress accumulates. TTHS is the threshold temperature (°C) above which Heat Stress accumulates, The equation used to calculate Weekly Heat Stress is expressed as: if Tmax > TTHS, then HS = (Tmax - TTHS) x THHS, if Tmax < TTHS, then HS = 0. The growth of A. niger has an extensive temperature range from 6 to 47 °C with a relatively high upper optimum of 35-37 °C

Fig. 1. Global distribution of A. niger and the Ecoclimatic (EI) Index of this species modelled by CLIMEX for current climate.

(Schuster et al., 2002; Hassouni et al., 2007; Mogensen et al., 2009; Astoreca et al., 2010; Shehu and Bello, 2011). The water activity limit for growth is 0.88, which is relatively high compared with other Aspergillus species. A. niger is able to grow over an extremely wide pH range: 1.4-9.8 with optimum levels between 4 and 6.5. These abilities and the profuse production of conidiospores, which are distributed via the air, secure the ubiquitous occurrence of the species, with a higher frequency in warm and humid places (Schuster et al., 2002; Samson et al., 2004; Gautam et al., 2010). In our study TTHS was set at 47 °C due to the fact that this is the temperature at which A. niger's physiological activities stop and THHS was set at 1.

• Growth index

The CLIMEX growth index constitutes the product of the temperature and moisture indices. The following parameters comprise the temperature index: DV0—low temperature limit, DV1—lower optimal temperature; DV2—upper optimal temperature; and DV3—high temperature limit. For A. niger, the range of DV0 should be between 6 and 20 °C (Esmaeili et al., 2013), and 10 °C was determined to provide the best fit to the observed distribution of A. niger. Summer temperatures in areas with the known records rarely exceed 45 °C (Esmaeili et al., 2014). And so, DV3 was established as 39 °C. The DV1 was established as 25 °C, as this is the documented low favourable temperature for A. niger (Parra and Magan, 2004). The DV2 was established as 35 °C as dependent on species' varieties, temperatures of up to 35 °C are suitable for A. niger (Parra and Magan, 2004) (Fig. 1).

• Moisture index

The following parameters comprise the soil moisture index in CLIMEX: SM0—the lowest threshold; SM1—the lower optimum moisture threshold; SM2—upper optimum moisture threshold; and SM3—the upper threshold. SM0 was established as 0.07 which represents the permanent wilting point, derived from observed distributions of A. niger in Iran, Afghanistan and Pakistan. SM1 was established as 0.08 and SM2 as 0.9, in order to include varieties grown in Italy, France, Germany and Greece. SM3 was established as 10 since higher soil moisture content has a negative effect on A. niger. These chosen values enabled the highest EI values within native distribution areas, in which the highest density of records were observed (Fig. 1).

2.5. A link between the parameters were used in CLIMEX and the environment that A. niger experiences

Because of aerobic nature of filamentous fungi like A. niger, they are usually found in the surface layers of soil where soil atmosphere is in exchange with air atmosphere above the soil. In this regard, parameters used in optimization process are

Fig. 2. Current and potential distribution of A. niger in the validation region based on EI index.

laboratory conditions which microorganisms are likely to experience in nature, exactly the same as those macro organisms such as animals, plants and other surface dwellers do (i.e., meteorological parameters that surface dwellers experience). The optimum growth parameters reported for A. niger by researchers have been all obtained in laboratory scale to be optimized and controlled in the field conditions. So, researchers use macro-climate parameters to find the optimum growth conditions of microorganisms; Refer to Esmaeili et al. (2013) and Esmaeili et al. (2014) for further information on A. niger and its environmental growth conditions. Aeration, in order to exchange gases between soil and air during biodegradation process using A. niger, is an essential factor to help the fungus to meet the oxygen need required for the process. In this regard, it should be mentioned that aeration not only provides oxygen for the fungus, but also prevents the process from getting anaerobic like some composting and other fermentation processes under anaerobic conditions. In addition, aeration would help thermal exchange between soil and atmosphere, and even help the fungus to adopt itself to atmospheric temperature. It should be stated that there is a relationship between soil and air temperatures. Annual mean soil temperature almost equals annual mean atmosphere temperature plus 1 (Siderius, 1973). Thus, meteorological variables used in the present study are acceptable. Furthermore, in the present study, moisture parameter is soil moisture levels derived from observed distribution of A. niger in different places. Therefore, it can be a suitable index to estimate future distributions of the fungus using the model. In general, considering oxygen requirement of A. niger, this strain would be in top layers of soil where it exists to fulfil for oxygen need and keep aerobic condition. This way, thermal exchange would happen between the soil atmosphere and air. So, using macro-climate parameters to run the model is justified and reasonable.

3. Results

• Historical climate and model validation

A comparison of global distribution with our A. niger climate suitability model (Fig. 1) indicates consistency of correlation of the modelled EI with the current global distributions. Climatic conditions suitable for A. niger are projected for Spain, France, eastern and western Iran, Congo, eastern Australia and South Africa. In that almost 93% of the A. niger records intersect with our model of global climate suitable for the species indicates the optimal nature of values chosen for all CLIMEX parameters (Fig. 1). The current distribution of A. niger in the United States was used as the basis of validation of our model (Fig. 2), and thus this region was omitted from model fitting. In the validation region, the model projects large parts of the central, eastern and south-eastern United States to be climatically suitable. It should be noted that in validation regions, almost 90% of the occurrence records intersected with the suitable categories (Fig. 2).

Fig. 3. Climate projections (EI) for A. niger using CLIMEX under the CS and MR GCMs running the A2 scenario for the designated years. The MR and CS outputs for each time period have been overlaid to extract common areas.

• Agreement between both GCM output results for A. niger

(1) 2030

Superimposing CS and MR GCM outputs shows a number of countries projected by both models to be of high suitability for this fungus, while many others will become marginal from the current unsuitable category (Fig. 3). Countries which indicate agreement between two different GCMs in areas that will become highly suitable for this fungus are Angola, Congo, South Africa, eastern United States, southern India, eastern China, and western and eastern Australia.

(2)2050

Combining the CS and MR GCM results for 2050 shows that areas located from 100°W to 90°W and areas between 30°N and 50°N in the United States, large areas of Congo, areas located from 40°E to 50°E and areas between 40°N and 50°N in Russia and areas located from 145°E to 148°E and areas between 40°N and 20°N in Australia will become marginally suitable or unsuitable for A. niger growth by 2050. Excluding the above mentioned regions, 94% of the areas projected to be marginal suitable by 2030 will remain marginally suitable till 2050 (Fig. 3). In should be mentioned that suitability of A. niger decreases when compared to 2030.

(3)2070

When the two model outputs were overlaid for 2070, large areas located from 100°W to 70°W and areas between 30°N and 50°N in the United States, large regions in central Mexico, 25°S to 20°S and 60°W to 50°W, large areas in most African countries, large areas located from 30°E to 80°E and areas between 40°N and 52°N in Russia and areas located from 145°E to 153°E and areas between 40°N and 20°N in Australia will become considerably less suitable for A. niger growth compared to 2050 and 2030 (Fig. 3).

(4) 2100

The agreement between the results of both GCM outputs for 2100 indicate that most of the countries in the African continent will become unsuitable for A. niger growth compared to 2070, 2050, 2030 and current time. Interestingly, large areas in eastern United States will become marginally suitable when compared to 2030 and 2050. In other words, the suitability for A. niger growth in the United States will have an eastward shift. Large areas located from 33°E to 60°E and areas between 50°N and 55°N in Russia will become marginally suitable compared to 2070. In addition, this model demonstrates that the high suitability will shift northward to include areas between 56°N and 65°N and areas located from 32°E to 90°E in Russia by 2100 (Fig. 3).

Fig. 4. Common climate projections (EI) for A. niger growth from present time up to 2100, using CLIMEX under the CS and MR GCMs running the A2 scenario. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

• Sustainable regions for A. niger growth from present time up to 2100

The intersection of the two GCM outputs for 2030,2050,2070,2100 and current time indicates areas that are suitable now and will remain suitable or increase in suitability in the future. Based on the model outputs and the current distribution of A. niger, a map with more accurate approximation of sustainable regions for A. niger growth from present time up to 2100 was produced (Fig. 4). Fig. 4 shows that central and eastern Argentina, Uruguay, southern Brazil, eastern United states, central Ethiopia and north eastern Oman will be highly sustainable for A. niger growth from present time up to 2100 (Fig. 4, red colour). Also, our modelling approaches projected a sustainable moderate suitability for A. niger in all European countries (Fig. 4, yellow) excluding Ireland, United Kingdom, northern Germany, Swaziland, Austria, Denmark, Sweden, Norway, Finland, Estonia, Latvia and Netherlands for the current century (Fig. 4, white).

4. Discussion and conclusion

Biodegradation of pure LDPE films through A. niger has been shown to be effective (Esmaeili et al., 2013,2014). Therefore, understanding climate change impact on this important fungus is critical to the future of waste management decision making and the economy. In this study we sought to assess the climate change impact on localities suitable for A. niger at a global scale over the periods 2030, 2050, 2070 and 2100 and mapped sustainable regions for A. niger growth from present time up to 2100.

There are similarities in the projection of areas of suitability for the growth of A. niger in the CS and MR GCM outputs. However, variations between the outputs are also evident. As an example, the MR model projects that areas located between 110°W and 120°W and 60°N and 70°N in the United States fall into the category EI > 20 for A. niger, while the CS model categorizes those areas as EI < 20 for 2100. Similar variance can be found in Spain, United Kingdom and Italy by 2100. Variations in results for areas of projected suitability for A. niger are considerable in certain cases and can be attributed to the differences in inherent assumptions and predictions in the two models, in terms of projected rates of change in rainfall and temperature. The MR model predicts an increase in temperature of 4.31 °C, in contrast to 2.11 °C in the CS model, by 2100 (Suppiah and Hennessy, 2007; Chiew et al., 2009). Predictions by the two models regarding future annual rainfall also differ, with the CS indicating a 13%-15% decrease, while the MR forecasts only a 1% reduction (Suppiah and Hennessy, 2007). Therefore, the refined projections through intersection techniques for each period of time (2030, 2050, 2070 and 2100) illustrated in Fig. 3 provide greater certainty with regard to areas projected to become highly or marginally suitable for A. niger growth than those achieved by the majority of earlier studies focused on other species and used a single GCM (Brklacich

and Stewart, 1995; Mearns, 1995; Luo et al., 2003). Results derived from a single GCM, while generally precise, are limited to projections valid only for that specific scenario and thereafter are purely speculative in terms of representing alternative future scenarios. While the outcomes in these single GCM studies have some application, they generate little information in terms of probable eventualities. Moreover, they provide no indications of how their results will match broader uncertainty ranges, or define these uncertainty ranges.

Our results provide insights into future climatic predictions for countries that can comprehensively rely on biodegradation method for plastic waste management through A. niger. This information is vital for most European countries, the United States, China, south-eastern South Africa, central Zambia, Rwanda, Burundi, central Kenya, central Ethiopia, northeastern Oman and Australia (Fig. 4). In this regard, we note that biodegradation is dependent on many factors, which includes the characteristics of the polymer, the type of organism, and the nature of pretreatment. Polymer characteristic variables such as mobility, crystallinity, tacticity, molecular weight, types of functional groups and constituents inherent in the structure and the qualities of plasticizers or additives added, are all factors in its effective degradation. However, the following should be considered when interpreting the results: Our modelling was purely climate-based and did not consider non-climatic factors such as land use, soil type, biotic interaction, competition and diseases. Current broad-scale climatic data was employed, and thus the results present purely broad-scale shifts, subject to the uncertainties surrounding future greenhouse gas emission levels.

Accurate projections of land use evaluation and climatic modelling are vital for effective long-term planning of waste management. From a social and economic perspective, utilization of our results to identify suitable regions for establishing landfills in areas highly suitable and remaining sustainable for microorganisms like A. niger will allow a significant cost reduction and improve the performance of biodegradation of LDPE over a long period of time through making use of natural climatic and environment factors. The results obtained here can be downscaled using finer resolution data where available to identify areas best suited for biodegradation sites based on local climatic conditions and landuse patterns.

There were, however, limitations that must be listed. CLIMEX outputs are climate response based, the impact of non-climatic parameters such as biotic interactions and inter-species competition were not taken into account. Thus, the following should be considered when interpreting the results; (a) In this study, the carbon dioxide enrichment and the potential genetic progress were not taken into account, meaning that adaptation of A. niger to future climate was not considered as this is a difficult exercise. (b) The modelling is only climate-based and does not take into account non-climatic factors such as use of land, type of soil, biotic interaction and competition. (c) Current broad-scale climatic data was employed, and thus results present purely broad-scale shifts. (d) Results are subject to the uncertainties surrounding future greenhouse gas emissions levels. (e) Although large parts of Africa were modelled to have suitable climatic conditions for A. niger in its current known distribution, limited data were available from these regions. This could be due to a shortage of reports from these areas.

References

Ababutain, I.M., 2013. Effect of some ecological factors on the growth of Aspergillus niger and Cladosporium sphaerospermum. Amer. J. Appl. Sci. 10,159-163. Abd El-Rehim, H., Hegazy, E.-S.A., Ali, A., Rabie, A., 2004. Synergistic effect of combining UV-sunlight—soil burial treatment on the biodegradation rate of

LDPE/starch blends. J. Photochem. Photobiol. A: Chem. 163, 547-556. Adams, R.M., Hurd, B.H., Lenhart, S., Leary, N., 1998. Effects of global climate change on agriculture: an interpretative review. Clim. Res. 11,19-30. Alavi Moghadam, M., Mokhtarani, N., Mokhtarani, B., 2009. Municipal solid waste management in Rasht City, Iran. Waste Manage. 29, 485-489. Al-Salem, S., Lettieri, P., Baeyens, J., 2009. Recycling and recovery routes of plastic solid waste (PSW): A review. Waste Manage. 29, 2625-2643. Ardestani, F., Kasebkar, R., 2014. Non-structured kinetic model of Aspergillus Niger growth and substrate uptake in a batch submerged culture. British Biotechnol. J. 4, 970.

Astoreca, A., Magnoli, C., Dalcero, A., 2010. Ecophysiology of Aspergillus section Nigri species potential ochratoxin A producers. Toxins 2, 2593-2605. Bai, R., Sutanto, M., 2002. The practice and challenges of solid waste management in Singapore. Waste Manage. 22, 557-567.

Bhalerao, T., Puranik, P., 2007. Biodegradation of organochlorine pesticide, endosulfan, by a fungal soil isolate, Aspergillus niger. Int. Biodeterioration Biodegrad. 59,315-321.

Bonhomme, S., Cuer, A., Delort, A., Lemaire, J., Sancelme, M., Scott, G., 2003. Environmental biodegradation of polyethylene. Polym. Degrad. Stab. 81, 441-452.

Bonner, J.T., 1948. A study of the temperature and humidity requirements of Aspergillus niger. Mycologia 728-738.

Brklacich, M., Stewart, R.B., 1995. Impacts of climate change on wheat yield in the Canadian prairies. In: Climate Change and Agriculture: Analysis of

Potential International Impacts. pp. 147-162. Central Pollution Control Board in New Delhi in India, 2013.

Chehri, J., 2013. Factors affecting the growth of biomass of Aspergillus niger. Med. Sci. Public Health 1, 1-5.

Chiew, F., Kirono, D., Kent, D., Vaze, J., 2009. Assessment of rainfall simulations from global climate models and implications for climate change impact on

runoff studies. In: 18th World IMACS Australia, pp. 3907-3914. Commission, M.M., 1998. Marine Mammal Commission: Annual Report to the Congress: 1997. Marine Mammal Commission. Dijkgraaf, E., Vollebergh, H.R., 2004. Burn or bury? A social cost comparison of final waste disposal methods. Ecol. Econ. 50, 233-247. Esmaeili, A., Pourbabaee, A.A., Alikhani, H.A., Shabani, F., Esmaeili, E., 2013. Biodegradation of low-density polyethylene (LDPE) by mixed culture of

Lysinibacillus xylanilyticus and Aspergillus niger in soil. PLoS One 8, e71720. Esmaeili, A., Pourbabaee, A.A., Alikhani, H.A., Shabani, F., Kumar, L., 2014. Colonization and biodegradation of photo-oxidized low-density polyethylene

(LDPE) by new strains of Aspergillus sp. and Lysinibacillus sp. Bioremediat. J. 18, 213-226. Finnveden, G., Johansson, J., Lind, P., Moberg, A., 2005. Life cycle assessment of energy from solid waste—part 1: general methodology and results. J. Cleaner Prod. 13, 213-229.

Gautam, A., Avasthi, S., Sharma, A., Bhadauria, R., 2010. Efficacy of Triphala Churn ingredients against A. niger and potential of clove extract as herbal fungitoxicant. Biol. Med. 2,1-9.

Grima, S., Bellon-Maurel, V., Feuilloley, P., Silvestre, F., 2000. Aerobic biodegradation of polymers in solid-state conditions: A review of environmental and physicochemical parameter settings in laboratory simulations. J. Polym. Environ. 8, 183-195.

Hang, Y., Splittstoesser, D., Woodams, E., 1975. Utilization of brewery spent grain liquor by Aspergillus niger. Appl. Microbiol. 30,879-880.

Harshvardhan, K., Jha, B., 2013. Biodegradation of low-density polyethylene by marine bacteria from pelagic waters, Arabian Sea, India. Mar. Pollut. Bull. 77,100-106.

Hassouni, H., Ismaili-Alaoui, M., Lamrani, K., Gaime-Perraud, I., Augur, C., Roussos, S., 2007. Comparative spore germination of filamentous fungi on solid state fermentation under different culture conditions. Micol. Apl. Int. 19,7-14.

Hiort, J., Maksimenka, K., Reichert, M., Perovic-Ottstadt, S., Lin, W., Wray, V., Steube, K., Schaumann, K., Weber, H., Proksch, P., 2005. New natural products from the sponge-derived fungus Aspergillus niger. J. Nat. Prod. 68, 1821-1821.

Hui, Y., Li'ao, W., Fenwei, S., Gang, H., 2006. Urban solid waste management in Chongqing: Challenges and opportunities. Waste Manage. 26,1052-1062.

IPCC, l.P.o.C.C., 2001. Climate change 2001: The science of climate change. Summary for Policymakers and Technical Summary of the Working Group I Report.

IPCC, l.P.o.C.C., 2007. Climate change 2007: Synthesis report. Summary for Policymakers.

Jakubowicz, I., Yarahmadi, N., Arthurson, V., 2011. Kinetics of abiotic and biotic degradability of low-density polyethylene containing prodegradant additives and its effect on the growth of microbial communities. Polym. Degrad. Stab. 96, 919-928.

Jakubowicz, I., Yarahmadi, N., Petersen, H., 2006. Evaluation of the rate of abiotic degradation of biodegradable polyethylene in various environments. Polym. Degrad. Stab. 91,1556-1562.

Jones, G., Thornton, K., 2003. The potential impacts of climate change on maize production in Africa and Latin America in 2055. Global Environ. Change 13, 51-59.

Kapri, A., Zaidi, M., Satlewal, A., Goel, R., 2010. SPlON-accelerated biodegradation of low-density polyethylene by indigenous microbial consortium. Int. Biodeterioration Biodegrad. 64, 238-244.

Kriticos, D., Potter, K., Alexander, N., Gibb, A., Suckling, D., 2007. Using a pheromone lure survey to establish the native and potential distribution of an invasive Lepidopteran. J. Appl. Ecol. 44, 853-863.

Lazarevic, D., Aoustin, E., Buclet, N., Brandt, N., 2010. Plastic waste management in the context of a European recycling society: comparing results and uncertainties in a life cycle perspective. Resour. Conserv. Recy. 55, 246-259.

Luo, Q., Williams, M.A., Bellotti, W., Bryan, B., 2003. Quantitative and visual assessments of climate change impacts on South Australian wheat production. Agric. Syst. 77, 173-186.

Magrinho, A., Didelet, F., Semiao, V., 2006. Municipal solid waste disposal in Portugal. Waste Manage. 26,1477-1489.

Mateescu, C., Buruntea, N., Stancu, N., 2011. Investigation of Aspergillus niger growth and activity in a static magnetic flux density field. Rom. Biotechnol. Lett. 16,6364-6368.

Mearns, L., 1995. Research issues in determining the effects of changing climate variability on crop yields. In: Climate Change and Agriculture: Analysis of Potential lnternational lmpacts. pp. 123-143.

Mogensen, J., Nielsen, K., Samson, R., Frisvad, J., Thrane, U., 2009. Effect of temperature and water activity on the production of fumonisins by Aspergillus niger and different Fusarium species. BMC Microbiol. 9, 281.

Mwanza, M., 2011. A comparative study of fungi and mycotoxin contamination in animal products from selected rural and urban areas of South Africa with particular reference to the impact of this on the health of rural black people. Faculty of Health Science, University of Johannesburg, South Africa.

Nanda, S., Sahu, S., Abraham, J., 2010. Studies on the biodegradation of natural and synthetic polyethylene by Pseudomonas spp. J. Appl. Sci. Environ. Manage. 14.

O'Brine, T., Thompson, R.C., 2010. Degradation of plastic carrier bags in the marine environment. Mar. Pollut. Bull. 60, 2279-2283.

Oladiran, A., Iwu, L., 1993. Studies on the fungi associated with tomato fruit rots and effects of environment on storage. Mycopathologia 121,157-161.

Ortiz, R., Sayre, KD., Govaerts, B., Gupta, R., Subbarao, G., Ban, T., Hodson, D., Dixon, J.M., Ivan Ortiz-Monasterio, J., Reynolds, M., 2008. Climate change: Can wheat beat the heat? Agric. Ecosyst. Environ. 126, 46-58.

Pappas, P.G., Alexander, B.D., Andes, D.R., Hadley, S., Kauffman, C.A., Freifeld, A., Anaissie, E.J., Brumble, L.M., Herwaldt, L., Ito, J., 2010. Invasive fungal infections among organ transplant recipients: results of the transplant-associated infection surveillance network (TRANSNET). Clin. lnfect. Dis. 50, 1101-1111.

Parra, R., Magan, N., 2004. Modelling the effect of temperature and water activity on growth of Aspergillus niger strains and applications for food spoilage moulds. J. Appl. Microbiol. 97, 429-438.

Pattison, R.R., Mack, R.N., 2008. Potential distribution of the invasive tree Triadica sebifera (Euphorbiaceae) in the United States: evaluating CLIMEX predictions with field trials. Global Change Biol. 14, 813-826.

Pearson, R.G., Dawson, T.P., Berry, P.M., Harrison, P.A., 2002. SPECIES: a spatial evaluation of climate impact on the envelope of species. Ecol. Modell. 154, 289-300.

Rebeiz, K., Craft, A., 1995. Plastic waste management in construction: technological and institutional issues. Resour. Conserv. Recycl. 15, 245-257.

Reddy, K.R., Hodges, H.F., McKinion, J.M., 1997. A comparison of scenarios for the effect of global climate change on cotton growth and yield. Funct. Plant Biol. 24, 707-713.

Reddy, M.S., Reddy, P.S., Subbaiah, G.V., Subbaiah, H.V., 2014. Effect of plastic pollution on environment.

Rogers, D.J., Reid, R.E., Rogers, J.J., Addison, S.J., 2007. Prediction of the naturalisation potential and weediness risk of transgenic cotton in Australia. Agric. Ecosyst. Environ. 119, 177-189.

Samson, R.A., Houbraken, J., Kuijpers, A.F., Frank, J.M., Frisvad, J.C., 2004. New ochratoxin A or sclerotium producing species in Aspergillus section Nigri. Stud. Mycol. 50, 45-61.

Schuster, E., Dunn-Coleman, N., Frisvad, J., Van Dijck, P., 2002. On the safety of Aspergillus niger—a review. Appl. Microbiol. Biotechnol. 59, 426-435.

Scott, G., 1999. Polymers and the Environment. Royal Society of Chemistry.

Shabani, F., Kotey, B., 2015. Future distribution of cotton and wheat in Australia under potential climate change. J. Agric. Sci. 1-11.

Shabani, F., Kumar, L., Esmaeili, A., 2014a. Future Distributions of Fusarium oxysporumf. spp. in European, middle eastern and north African agricultural regions under climate change. Agric. Ecosyst. Environ. 197, 96-105.

Shabani, F., Kumar, L., Nojoumian, A.H., Esmaeili, A., Toghyani, M., 2015. Projected future distribution of date palms and its potential use in alleviating micronutrient deficiency. J. Sci. Food Agric..

Shabani, F., Kumar, L., Taylor, S., 2012. Climate change impacts on the future distribution of date palms: a modeling exercise using CLIMEX. PLoS One 7, e48021.

Shabani, F., Kumar, L., Taylor, S., 2013. Suitable regions for date palm cultivation in Iran are predicted to increase substantially under future climate change scenarios. J. Agric. Sci. 543-557.

Shabani, F., Kumar, L., Taylor, S., 2014b. Distribution of date palms in the middle east based on future climate scenarios. Camb. J. Exp. Agric. 244-263.

Shabani, F., Kumar, L., Taylor, S., 2014c. Projecting date palm distribution in Iran under climate change using topography, physicochemical soil properties, soil taxonomy, land use and climate data. Theor. Appl. Climatol. 152,543-557.

Shah, A.A., Hasan, F., Hameed, A., Ahmed, S., 2008. Biological degradation of plastics: a comprehensive review. Biotechnol. Adv. 26, 246-265.

Sharma, R., 2012. Pathogenecity of Aspergillus niger in plants. Cibtech J. Microbiol. 1, 47-51.

Sheavly, S., Register, K., 2007. Marine debris & plastics: environmental concerns, sources, impacts and solutions. J. Polym. Environ. 15, 301-305.

Shehu, K., Bello, M., 2011. Effect of environmental factors on the growth of Aspergillus species associated with stored millet grains in Sokoto. Nigerian J. Basic Appl. Sci. 19.

Siderius, W., 1973. Soil transitions in central east Botswana (Africa). lnternational lnstitute for Aerial Survey and Earth Sciences.

Song, J., Murphy, R., Narayan, R., Davies, G., 2009. Biodegradable and compostable alternatives to conventional plastics. Philos. Trans. R. Soc. B 364, 2127-2139.

Suppiah, R., Hennessy, K., 2007. Australian climate change projections derived from simulations performed forthe IPCC 4th Assessment Report. Australian

Meteorological Magazine, pp. 131-152. Sutherst, R.W., Maywald, G., Kriticos, D.J., 2007a. CLIMEX version 3: User's guide. In: Ltd, H.S.S.P. (Ed.), Melbourne.

Sutherst, R.W., Maywald, G.F., Bourne, A.S., 2007b. Including species interactions in risk assessments for global change. Global Change Biol. 13,1843-1859. Yang, J., Song, Y., Qin, X., 2007. Biodegradation of polyethylene. Huan jing ke xue= Huanjing kexue/[bian ji, Zhongguo ke xue yuan huan jing ke xue wei

yuan hui'' Huanjing ke xue'' bianji wei yuan hui.] 28,1165-1168. Zahra, S., Abbas, S.S., Mahsa, M.-T., Mohsen, N., 2010. Biodegradation of low-density polyethylene (LDPE) by isolated fungi in solid waste medium. Waste Manag. 30,396-401.