The effects of temporal and spatial variations in food resources on the distribution and abundance of Black-necked Cranes, Grus nigricollis

doi:10.21203/rs.3.rs-4104304/v1

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The effects of temporal and spatial variations in food resources on the distribution and abundance of Black-necked Cranes, Grus nigricollis

https://doi.org/10.21203/rs.3.rs-4104304/v1

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The Black-necked Crane, Grus nigricollis, is categorized as Vulnerable on the IUCN Red List. Food distribution and biomass are factors that will determine its long-term survival. Understanding food variation will facilitate the development of effective conservation plans for the protection of this vulnerable species. Available biomass of food for Black-necked Cranes was sampled on the agricultural farmlands and grasslands used by foraging flocks of these species in Dashanbao Nature Reserve, during the winter periods of 2012 and 2015. We compared variation separately in biomass of a particular group (e.g. invertebrates, grains and potato) and analysed the relationship between food biomass utilisation by cranes. The results showed that relative availability of invertebrates in grassland, and potato and grain in farmland, varied seasonally. The number of cranes was less affected by the monthly food variation in the reserve. However, the habitat type has an impact on the number of cranes. In grassland habitat, crane abundance was positively related to invertebrate biomass. However, there was no significant correlation in farmland habitat. Availability food in both habitats vary across years, months, which relate to a seasonal crop depletion and farming, and annual to crop productivity, and invertebrate availability, influenced in part by winter temperatures. Therefore, we recommend that there should be enough food biomass in the reserve for cranes to forage during the cold-weather periods, and expanded grassland foraging habitat, so as to expand the range of foraging and increase the diversity of food for the cranes.

Black-necked Crane

biomass

food distribution

temporal and spatial patterns

flock density

Food availability, climate, landscape topography, predation risk and vegetation characteristics can affect the distribution and relative abundance of birds at multiple scales (Murkin and Kadlec 1986; Kalejta and Hockey 1994; Rey 1995; Johnson and Sherry 2001; Moegenburg and Levey 2003; Mengesha and Bekele 2008; Pugesek, et al. 2013; Chatterjee and Basu 2018, Zhang and Wang 2018). The impact of food abundance on bird distribution and diversity has been investigated for farmland birds by Sauerbrei et al. (2014), and for frugivorous and insectivorous birds by Blendinger et al. (2012), Wunderle et al. (2014) and Mackay et al. (2018). Some overwintering waterbirds also show greater species diversity where food is more abundant. For example, Alonso et al. (1994) pointed out there was a significant correlation between the minimum number of Common Cranes Grus grus and the availability of cereal food in the middle of winter (from December to January). The density of waterfowl is positively related to seed abundance in paddy field plots (Lee et al. 2007; Nam et al. 2012; Shimada et al. 2002; Yoo et al. 2008).

In addition to the amount of food available, the flexibility of birds' feeding strategies can affect the change of food resources for non-breeding waterbirds. The different feeding strategies of birds may end up partitioning the resources, and thus reducing the amount of food available for each individual species (Rotenberry and Wiens 1980; Alatalo 1980; Hutto 1981). Birds can change their feeding behavior and food choices by looking for alternative food, or leaving places with less food abundance. The plasticity of this behavior enables migratory birds to exploit unfamiliar or unpredictable habitats they encounter (Petit 2000).

Winter temperature may affect the change of food resources for non-breeding waterbirds. For example, the distribution of Mallard (Anas platyrhynchos) in winter is affected by temperature, duration of flood and snow depth, at least on a regional scale (Heitmeyer 2006; Schummer et al. 2010). Water level affects the habitat and food intake of Eurasian Teal Anas crecca and Eurasian Wigeon A. penelope, thus affecting the distribution of the two birds (Therkildsen and Bregnball 2006).

For cranes, there are few studies on the relationship between their distribution patterns and the abundance of their food. Hooded Cranes (Grus monacha) have been studied (Yang et al. 2015), with a focus mainly on the relationship between different food types and crane abundance. This study proposes that there is a correlation between food abundance and crane abundance. However, it is still unclear how changes in food abundance in different habitats affect the wintering abundance of Black-necked Cranes. Black-necked Cranes, which are categorized as Vulnerable on the IUCN Red List and listed in Appendix I of CITES. Black-necked Cranes is a flagship species that lives its their entire life on high plateaus, primarily wintering in the Qinghai-Tibet and Yunnan-Guizhou Plateaus. Black-necked Cranes mainly forage in the farmlands-grasslands to obtain different types of food (Dong 2016) and they also go to wetlands to find food, drink water or rest, and sleep in shallow water at night in Dashanbao National Nature Reserve (hereafter referred to as Dashanbao Reserve). Dashanbao Reserve is listed as a wetland of international significance under the Ramsar Convention on Wetlands. It is the main stopover and wintering area for the eastern population of Black-necked Cranes, and is also an important habitat for other waterfowl. There are between 1100 and 1200 Black-necked Cranes in Dashanbao Reserve (about one-eighth of the total world population) in 2012–2015. Dong et al. (2016) reported that the crane’s diet in the reserve consists primarily of domestic food crops such as 74% grains overall (and it gets all of these grains from farmland) and potatoes (8%) overall in farmland and invertebrates (14%, earthworms, coleopteran larvae) in grassland. A much smaller proportion of the diet is comprised of turnips and wild herbaceous plants and tubers. We found that Black-necked Cranes also feed on invertebrates in farmland and nocturnal wetlands. The important nocturnal wetland roost is DaHaizi in Dashanbao reserve, with about 50% of the black-necked cranes nocturnally roosting there.

Kong et al. (2008) reported that time spent foraging was mostly in arable farmland and natural grassland and there were no significant difference in time spent foraging between these two habitats. Dong et al. (2016) reported a much smaller proportion of the diet was comprised of wild herbaceous plants and tubers in wetland areas. As the Black-necked Crane forages in multiple habitats in Dashanbao Reserve, we explore how changes in food biomass in multiple habitats affect the abundance and distribution of Black-necked Cranes in winter. In this paper, we examine the temporal and spatial variation in the abundance of different food types in multiple habitats and the distribution of cranes, which can provide a deeper understanding of habitat use for cranes, and provide a theoretical basis for the protection of Black-necked Cranes in future.

Study site

Dashanbao Reserve is located in Zhaotong City, Northeast Yunnan Province (103° 15′–103° 24′ E; 27° 18′–27° 29′ N, altitudes of 3,000–3,200 m, Fig. 1). The study area is a warm, humid plateau with a monsoon climate characterized by cool, wet summers (May-Jul) and cold, dry winters (Dec-Mar). During winter, frequent days of sustained freezing temperatures can be expected from December to January. The mean temperature for January is 1℃, for July is 12.7℃. The mean annual temperature is 6.2℃, with 123 frost-free days and 34.6 snow-cover days/year. The average snow cover is about 3–4 cm. The mean annual precipitation is 1,165 mm (Li and Zhong 2010). There are four main reservoirs in Dashanbao Reserve: Dahaizi, Tiaodunhe, Lelizhai and Yanmaidi. Dahaizi reservoir has a low water level and a large area of shallow water and surrounding wetlands. This is the area within Dashanbao reserve where Black-necked cranes mainly congregate in winter, with many also in the area around Tiaodunhe. The water storage areas of Lelizhai and Yanmaidi reservoirs are small, and few Black-necked cranes are found around them. So our study sites mainly focused on Dahaizi and Tiaodunhe. Arable farmland (henceforth referred to as farmland) included fields of cereal (Avena sativa and Fagopyrum tataricum), potatoes (Solanum tuberosum) and turnip (Brassica rapa var. rapa). Avena sativa, potatoes and turnip were planted in March of each year, and buckwheat (Fagopyrum tataricum) was sown one month later than oats and potatoes. Oats, buckwheat, potatoes and turnip, an annual ripening, the crop is harvested in July-August each year. Natural grassland (henceforth referred to as grassland) comprised meadows with minimal water (Kong et al. 2011) and dominated by orchard grass (Dactylis glomerata), bluegrass (Poa annua), Leontopodium, Trifolium, Pterospermum heterophyllum, Pedicularis densispica, Luzula multiflora, Hemiphragma heterophyllum (Kuang et al. 2008). Marsh comprised both wetlands around the lake and meadows with large areas of water. According to the estimation of animal husbandry department, the livestock carrying capacity of grassland is 26,000 sheep units in reserve (the number of sheep units that can be supported on 1hm² of grazed grassland during the annual grazing period). There are more than 40,000 sheep units on 19,200 hm² in the reserve, far exceeding the carrying capacity.

Distribution of foraging cranes

We selected three transect routes crossing the mountain ridge of the reserve at two sites which supported the largest flocks of cranes according to the reserve staff’s experience and the suggestions from previous research in October 2013 (Kong et al. 2011). The majority of cranes arrived in early November and remained feeding in farmland and grassland in Dashanbao Reserve until early March. In case of severe weather such as fog and snow, observations were postponed for one day. We observed cranes for three days every week for 15 weeks between the second week of November and the end of February. Along the three survey lines (Fig. 1), we recorded crane group size and we observed the number of crane individuals in each group. We recorded the feeding location by handheld GPS, and imported it into Google maps. Dashanbao habitat map (provided by Dasanbao Nature Reserve Administration, see Fig. 1) included marshes, grasslands, farmlands, freshwater, forests, and villages, we imported the sites on Google map into AcrGis 9.3, used the patch area of foraging habitat in the software, and obtained the area (km²) of foraging activity areas in different habitats pooled for a monthly estimate. The habitat map consists of small, uniformly shaped tiles, such that the area of land used by cranes can be judged by the number of patches a flock covered.

The main food types for crane were grains, potatoes in farmland, and invertebrates in the grassland, farmland and wetland in Dashanbao reserve. We used quadrat surveys of food availability in 40 fields using the transect line in farmland (Fig. 1). Ten quadrats (50×50×10 cm deep) were placed equidistantly along a diagonal transect across each field. One set of 176 quadrats was placed on the ground in the grain fields, another 222 quadrats were placed in the potato fields. Second, grassland polygons were more variable than agricultural fields so we followed the 9-point equidistantly sampling method of the inverted W-pattern in the field survey (Thomas 1985), and 295 quadrats were placed in the grassland (sampled monthly for eight months over two years), 110 quadrats were placed in the wetland in Dashanbao reserve. The proportion of grain, potato, grassland, and wetland fields that we sampled reflected the proportion of those land cover types in the crane use areas. We picked up cereal grains on unploughed plots. The second method turned all the soil for sampling all cereal grains and all potatoes on ploughed landsin farmland, and invertebrates (e.g., earthworms and Coleoptera larvae) larger than approximately 4 mm because that appeared to be the minimal size consumed by the cranes (Dong et al. 2016) in grassland, farmland and wetland within a depth of 10 cm due to the length of a crane’s bill is 12.4 cm (Dong et. al 2016). The counts and the available biomass of all food types in each quadrat were recorded. The extracted food items were stored in plastic bags and frozen until processing. After defrosting, cereals, potatoes, invertebrates were separated, dried (60℃, 48 h) and then weighed to determine dry biomass (0.001 g precision).

Analysis

We used the whole area in which foraging occurred to record the number of cranes, and we identified the foraging habitat types used by the cranes and divided these foraging locations into crane foraging habitat types during each wintering period. The flock density (No./km²) of wintering Black-necked cranes in habitat i was the number of individuals in habitat farmland or grassland, divided by the area in which foraging activities took place in that habitat. The area used by cranes can be judged by the number of patches a flock covered in habitat map. The proportional abundance (a) of wintering Black-necked Cranes in habitat i was expressed as a = Ni / N, where N was the number of cranes recorded on the reserve. The biomass (g) of food resources is defined as of food (0.25 m²).

Understanding temporal changes in foods available to these wintering birds is important here to assess how rapidly foods are depleted over the winter. We used ANOVA to compare food biomass among months and used chi-square test to compare food biomass between habitats. We present weights of three types of food for invertebrates, grains (oats and buckwheat), and potatoes. If the data did not meet the homogeneity of variance requirement after transformation were used to test the differences within the group. In order to determine the relationship between the wintering periods and habitat types of Black-necked Crane, and the changes in food mass, a general linear model was used to analyze the effects of habitat types and their interactions on the relative densities of Black-necked Cranes during wintering. Linear regression was used to analyze the linear relationship between the mass of food resources and the flock density of Black-necked Cranes. Where this relationship was statistically significant, it was analysed in further detail to assess whether the nature of the relationship varied between different habitats, or within different months of the year, applying a Bonferroni correction for multiple tests to the P values. Measures of the density of Black-necked Cranes, and of the biomass of food resources, were logtransformed (log (x + 1)).

Temporal and spatial variation of food

The mean number of invertebrates on farmland was about 2 ± 0.10 items/0.25m² (N = 121) and on grassland 23 ± 3.09 items/0.25m² (N = 103), on wetland 12 ± 1.02 items/0.25m² (N = 108). We observed that the invertebrate abundance in DaHaizi wetland were about 4 items/0.25 m² (N = 45). We found that the black-necked cranes distributed in Dahaizi wetland mainly fed on grassland and agricultural land. The biomass of potato in farmland was no inter-annual differences (Table 1, Fig. 2). In the case of grain, intergroup analysis showed that the available food biomass in 2014–2015 was higher than that in 2012–2013 (F_2,214 = 11.03, P < 0.001) and 2013–2014 (F_2,060 = 10.22, P < 0.001) (Fig. 3). The biomass of main foods (invertebrates) in grassland was no inter-yearly differences (Table 1, Fig. 4). Available food biomass in grassland was lower in 2013–2014 than in 2012–2013 and 2014–2015 (Fig. 4).

The biomass of main foods in farmland was inter-monthly differences for several food groups (Table 1, Fig. 5). The biomass of potato and grain on farmland gradually decreases from November to February, with the highest biomass of potato in March (Fig. 5) and grain in November (Fig. 6). In grassland, the biomass of main foods (invertebrates) in grassland was inter-monthly differences (Table 1, Fig. 7). Available invertebrate biomass in November was higher than these in the other four months (Fig. 7). Separate comparisons of the four food biomasses between sites showed no differential differences (Table 1).

Table 1

Statistical differences in different food types between years, months, locations, and habitats. Bolded P-values are those where α < 0.05.
food type	year		month		site
	F	P	F	P	F	P
potato	0.132	0.877	55.879	0.001	0.452	0.502
grain	3.896	0.022	6.952	0.001	0.697	0.405
invertebrate	1.122	0.327	6.673	0.001	3.935	0.05

Food abundance and flock density of Black-necked Cranes

The flock density of Black-necked Cranes in farmland was 76 /km² while in grassland was 11 /km² averages over all 8 months, respectively. The flock density of Black-necked Cranes fluctuated during the wintering period, but less affected by the monthly variation. However, the habitat type has an impact on the number of cranes (F_1,490 = 17.503, P < 0.001). The density of Black-necked Cranes in farmland from November to January gradually increased, however, in February decreased to the lowest point and then increased to the highest point in March, while the flock density of Black-necked Cranes in grassland showed the opposite pattern (Fig. 8). The density of Black-necked Cranes in grassland increased the highest point in November, from November to January gradually decreased, decreased to the lowest point in January, and gradually increased in February and March (Fig. 8). The results of linear regression analysis showed that the flock density of Black-necked Cranes was significantly positively correlated with available food biomass (Table 2, Fig. 9). In grassland, the density of Black-necked Cranes was positively correlated with the amount of available food biomass (Table 2, Fig. 10). In farmland, there was no correlation between the density of Black-necked Cranes and their available food biomass (Table 2, Fig. 11).

Table 2

The effects of available food and total food abundance in farmland and grassland and combined two habitat on the Black-necked Crane abundance and density by linear regression.
	Effect	Regression coefficient (± s.e)	Standardized regression Coefficient	t	P
Combined habitat	No. cranes/km²
	Constant	3.036 ± 0.144		21.129	0.000
	Mean mass of available food (g/0.25m², dry mass) of main foods	0.038 ± 0.012	0.468	3.266	< 0.05
Grassland	No. cranes/km²
	Constant	2.121 ± 0.291		7.297	0.000
	Mean mass of available food (g/0.25m², dry mass) of main foods	0.308 ± 0.125	0.502	2.466	< 0.05
Farmland	No. cranes/km²
	Constant	3.756 ± 0.119		31.613	0.000
	Mean mass of available food (g/0.25m², dry mass) of main foods	0.010 ± 0.007	0.322	1.444	0.166

Our result showed greater crane densities are supported in farmland fields in all months compared to that in grassland. We suggest that cranes obtain more biomass of farmland food than in grassland. Their densities were not influenced by the variability in biomass of available farmland foods there. Densities of foraging cranes however were responsive to invertebrate availability in grasslands. Availability food in both habitats vary across years, months, which relate to a seasonal crop depletion and farming, and annual to crop productivity, and invertebrate availability, influenced in part by winter temperatures.

Temporal and spatial variation of food in farmland

Annual differences in availability of different food types in farmland related to growing conditions. The annual difference in grain may be due to damage by spring freezing in 2012–2013 and 2013–2014. The grain harvest in 2014–2015, by contrast, was ideal, so the food biomass in this period is higher than it was in the previous two years. We suggest that distribution of cranes was affected by inter-annual variation in abundance or availability of different food types.

Monthly difference in availability of different food types in farmland relate to depletion of foods by foraging cranes, timing of farming practices. The monthly difference for potatoes is probably due to the fact that potatoes are planted in March, so that the food biomass in this period is significantly higher than in other months. The monthly difference in grains was similar to that in potato, and newly planted oat in late March, so the decrease in food biomass in January and February was more obvious than it was in November and March. There is no difference in four food group between the two sites, which also indicates that the Black-necked Cranes follow the same crops in both sites. The abundance of invertebrates in farmland less than grassland may be related to the ploughing of the soil and spraying of pesticides on farmland, as well as changes in plant species composition, particularly the conversion of traditional crops to cash crops in some parts of farmland in Dashanbao (Dong et al. 2023), or other aspects of the microhabitat, all of which have an impact on farmland invertebrate populations. The lower number of invertebrates in wetlands than in grassland in the Dashanbao Reserve may be related to the siltation of the wetlands, depriving insect larvae of survival conditions, which also threatens the animal food sources of the Black-necked Cranes (Hu et al. 2002).Although the availability of crop food (grain and potato) in January and February was lower than in other months, the density of cranes did not decrease in January, but began to decrease in February and increased significantly in March. Dong et al. (2016) speculated that the availability of food (invertebrate populations) sharply declined in December and January due to the low temperature, which makes Black-necked Cranes choose more crop food during this period. Cranes were foraging in farm fields in spring, at high densities, and apparently overlapping with seeding of potatoes and grains. Newly seeded potatoes in March were the reason for the sudden increase in that food in March. We found the biggest contributor to food biomass was potato, and the population of cranes at Dashanbao is swelled by spring passage of these birds. Cranes feeding on newly seeded fields made crop damage and caused human-crane conflict.

Nam et al. (2012) and Schlacher et al. (2014) divided farmland into four levels to measure the impact of food biomass on the distribution of waterbirds. They reported that the paddy stalks in paddy fields would affect the distribution of waterbirds. Our study did not divide the farmland into several levels for comparison, but only verified the food factors on the density of the Black-necked Cranes in Dashanbao Reserve. The influence of other, non-food factors on the distribution and the density of Black-necked Cranes in this habitat requires further research.

Factors influencing invertebrate availability

Our results on invertebrate abundance in arable land less than grassland are similar to those of Hu et al. (2002). In grassland, low temperatures result in changes to invertebrate behaviour and soil properties, making invertebrates less accessible to foraging cranes in winter (Esselink and Zwarts 1989; Zwarts and Wanink 1993; Durell 2000). In our study area, invertebrate availability to cranes is likely to be lowest in December and January, when temperatures are lowest. Due to the relatively high temperature in November and the rising temperature in February, these months will show higher biomass of invertebrates than other months. Kong et al. (2011) pointed out that the activity depth of insect larvae in March was significantly less than in other months, which made the food more available. Our results showed that the biomass of insects was not at its highest, which may be related to the sampling time. Although March is also a period of temperature increase, our sampling usually took place in the late stage of migration (at the end of March); whether this phenomenon is related to the emergence of mature larvae into adults needs further research. On a smaller scale, the choice of feeding habitat is complex, not dependent on food density or habitat physical properties, and may be affected by (predation risk, flocking behaviour, competition, familiarity etc.). In contrast, Grant (1974) found bird distribution differed between rough and compacted soil. Uncompacted and soft sediment not limit the distribution of invertebrate. However, we found that the invertebrate in soft sediment in grassland is abundance than compacted sediment. Kong et al. (2011) also pointed out that a large number of Black-necked Cranes would choose to feed on grassland because there are abundant insect larvae in grassland. However, Black-necked Cranes foraging on underground invertebrates in grassland habitat are easily affected by the temperature during the overwintering period (Dong et al. 2016). We suggest that the cranes likely prefer invertebrates over grains, potentially because invertebrate organisms provide a greater source of protein and calcium than available in farmland food (such as grains, potatoes).

Food biomass and flock density of Black-necked Cranes

Our results verified the correlation between food biomass and crane proportional abundance to a certain extent in grassland. However, the biomass of food is not always followed by birds. There was no significant correlation between the flock density of Black-necked Cranes and the food biomass in farmlands during the middle of winter. This result differed from previous studies (Alonso et al. 1994). However, the results in agricultural land are similar to the findings of some other studies that there is no obvious correlation between the relative abundance of frugivorous birds and the abundance of their food (Malizia 2001; Marra 1998; Anderson 2004). These authors suggest that this may be due to lack of communication between birds of the same species, or the lack of complete information about the spatial distribution of food, or the change in distribution of different food types. Moreover, if food resources are sufficiently abundant then other factors (e.g. proximity to safe roosting places, proximity to conspecifics, avoidance of disturbance or risk of predation) could play a greater role in determining distribution of birds than food does.

We agree with cranes do not get complete information about the spatial distribution of food or the change in different food types. The reasons are as follows: firstly, the planting pattern of agricultural crops is generally concentrated in large areas, and the amount of food resources are relatively spatially inequality, which these choices are based on incomplete and imperfect information. Secondly, cranes foraging decisions are likely to be based on energy and nutritional content, time and energy spent finding food items, and then processing them (Pyle et al. 1977). Finally, at Dashanbao, the black-necked cranes arrive in November and leave until March of the following year, and the number of black-necked cranes also shows seasonal changes.

Management implications

Our result showed the spatial and temporal variation of crane habitat use is flexible enough for the variation in food biomass. The distribution of cranes is affected by variation in the availability of invertebrate prey in grassland, but that this is not the case in farmland. This may be related to the decrease of temperature in the middle of winter, which affects the availability of invertebrate food in grassland. Moreover, the types of food were very different in their energetic value, nutrients and ease with which they can be accessed and processed between farmland and grassland. We recommend that the protection administration should supplement additional foods (for example harvested, unplowee) for cranes during the cold-weather periods (from December to January), and restore grassland foraging habitat. This would benefit the farmers by reducing economic losses resulting from the cranes feeding on newly planted crop seeds during their late spring migration (in March). To further ease the conflict between cranes and local farmers, it is advisable to cultivate crops (potato) in a certain area that may be left unharvested for the cranes to eat.

Ethical Approval

Our research on Black-necked Cranes in Dashanbao National Nature Reserve was approved by the Chinese Wildlife Management Authority and conducted under Law of the People’s Republic of China on the Protection of Wildlife (August 28, 2004). The Administration of ZhaoTong Forestry Bureau approved our study on behavior observation and food availability sampling in the research plot in Dashanbao National

Nature Reserve (IDZTL2008163).

Competing interests

The authors declare that there is no conflict of interest.

Funding

This work received financial support from the Funding Natural Science Foundation of the Jiangsu Higher Education Institutions of China (grant #19KJB180028) and the Natural Research Foundation for Advanced Talents of Taizhou university (grant QD2016044).

Availability of data and materials

Not applicable.

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No competing interests reported.

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The effects of temporal and spatial variations in food resources on the distribution and abundance of Black-necked Cranes, Grus nigricollis

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Version 1

Abstract

Figures

Introduction

Methods

Study site

Distribution of foraging cranes

Analysis

Results

Temporal and spatial variation of food

Food abundance and flock density of Black-necked Cranes

Discussion

Temporal and spatial variation of food in farmland

Factors influencing invertebrate availability

Food biomass and flock density of Black-necked Cranes

Management implications

Declarations

References

Additional Declarations

Status:

Version 1