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Article

Bird Communities and the Rehabilitation of Al Karaana Lagoons in Qatar

by
Ayaterahman Draidia
1,†,
Momina Tareen
1,†,
Nuran Bayraktar
1,
Emily R. A. Cramer
2 and
Kuei-Chiu Chen
3,*
1
Department of Medical Education, Weill Cornell Medicine-Qatar, Education City, Qatar Foundation, P.O. Box 24144, Doha, Qatar
2
Sex and Evolution Research Group, Natural History Museum, University of Oslo, P.O. Box 1172, Blindern, 0318 Oslo, Norway
3
Department of Premedical Education, Weill Cornell Medicine-Qatar, Education City, Qatar Foundation, P.O. Box 24144, Doha, Qatar
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Birds 2022, 3(4), 320-340; https://doi.org/10.3390/birds3040022
Submission received: 18 July 2022 / Revised: 21 September 2022 / Accepted: 21 September 2022 / Published: 27 September 2022
(This article belongs to the Special Issue Feature Papers of Birds 2022–2023)
Browse Figures
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Abstract

:

Simple Summary

Qatar is located along the course of the African–Eurasian Flyway, a key migratory path for many bird species. Years of untreated waste delivery to the wastewater ponds at Al Karaana Lagoons in Qatar began to pose an environmental concern due to the build-up of contamination. As a result, the ponds were reconstructed and underwent environmental remediation. In this study, bird biodiversity before and after the remediation of Al Karaana Lagoons was documented, and the observed changes were analyzed. An increase in bird biodiversity was detected, including both migratory and resident species. Water from the TSE (treated sewage effluent) ponds was analyzed and showed gradual improvement following remediation in supporting bird life. The success observed in restoring Al Karaana Lagoons demonstrates the potential of reclaimed lands in preserving and promoting bird life, both in Qatar and, more broadly, around the world. We recommend continued monitoring of the TSE ponds and implementation of guidelines that aim to create a balance between habitat quality and human activities at the site.

Abstract

Qatar, a peninsular country in the Persian Gulf, is significant to avian species due to its location along the African–Eurasian Flyway, a key migratory path. Receiving untreated domestic and industrial liquid waste from Qatar in the past, Al Karaana Lagoons have since been reconstructed as an artificial wetland to address the growing environmental concern posed by contamination build-up. This study documents the changes in biodiversity at Al Karaana Lagoons following their environmental remediation. Data collected (2015 and 2017) by Ashghal (Public Works Authority) prior to project implementation was analyzed alongside data collected independently following project completion (2019–2021). There was a marked increase in bird biodiversity following remediation, including substantial use by migratory species and resident breeders. Further analysis of water quality data of the TSE (treated sewage effluent) ponds shows that they are eutrophic but still support substantial bird life. The project’s success demonstrates how reclaimed lands can provide important habitats to local and migratory birds and encourages similar restoration efforts in the future in both Qatar and elsewhere. We call for the continued monitoring of the site and the implementation of guidelines for the use of the site that balance human activities and habitat quality.

1. Introduction

Natural wetlands are highly diverse ecosystems that greatly benefit both their wildlife and the environment, from promoting biodiversity and providing habitats to acting as a carbon sink and wind buffer [1,2]. Many studies have demonstrated that artificial—or constructed—wetlands also provide ecosystem services, as do wetlands restored after human perturbations [3,4,5,6,7,8,9]. Specifically, artificial and restored wetlands can host similar levels of vertebrate species diversity compared to wetlands that have not been substantially impacted by human activity [4,7,8,9], although the abundance of individuals may be lower overall in artificial wetlands [8]. While full ecosystem function and, particularly, plant and macroinvertebrate communities may be slow to develop or recover after wetland construction or rehabilitation, use by highly vagile animals such as birds may recover quite quickly [4,5]. Since human activity has damaged or destroyed up to about 50% of wetland habitats globally [10,11], understanding how wetland construction and restoration function is important for the conservation of biodiversity.
Notwithstanding their potential conservation importance, artificial wetlands are often constructed as a measure for managing and purifying wastewater [2,12]. Such artificial wetlands can then occur in relatively novel locations. For example, Qatar has an arid desert environment, with approximately 80 mm of annual rainfall, but it is now home to several inland wetlands due to wastewater management and agricultural runoff (personal obs.). The country hosts 73 resident bird species and is an important stopover and over-wintering point in the African–Eurasian Flyway bird migratory route, used by an additional 211 species [13]. How these artificial wetlands are used by Qatar’s avifauna has not previously been studied.
In this study, we focus on one artificial wetland, Al Karaana Lagoons, in Qatar. Up until recently, the continuous discharge of untreated domestic and industrial waste that created and maintained Al Karaana Lagoons posed a growing environmental concern (Figure 1). Over time, the increasing build-up of contamination began to pose serious safety risks to local staff as well as birdwatchers who frequented the area. Additionally, the spreading contamination of the ponds produced foul smells and posed safety risks associated with sewage transport (Figures S1 and S2) [14]. The lack of lining in the pond basins was also a cause for concern as groundwater resources were potentially infiltrated by contaminant seepage. Extensive remediation and rehabilitation of the site were therefore conducted from 2015 to 2019 (detailed in the Section 2). The effects of the remediation in Al Karaana Lagoons on biodiversity and the bird populations, in particular, are the concern of this study. Previous studies have detailed the negative effects of wastewater on the diversity and abundance of different animal species [15,16]. Perhaps surprisingly, some studies that center around crab species that have a strong physiological tolerance for wastewater show increased abundance as well as improved potential fertility and embryo quality in wastewater [15,17]. As to Al Karaana, we assume that the pollutants negatively impacted the community prior to rehabilitation.
Considering the success of previous wetland restoration projects [7,9], we hypothesize that species diversity would increase following the restoration work (comparing Figure S3 to Figure S2 for habitant change). Further, we hypothesize that species diversity and individual abundance would continue to increase as the ecosystem becomes more mature following rehabilitation [18]. We further explore whether changes in individual abundance are related to the ecological niche and migratory status of the species [8,9]. Given the known use of nearby countries by migratory birds [19,20] and that artificial and restored wetlands are often used by migratory species [6,8], we further hypothesize that migratory species would utilize the area as a stopping-over site. Specifically, we predict that species diversity would increase in the spring and fall, relative to summer and winter, due to the presence of migratory species on the stopover. Finally, we compare diversity and abundance patterns across the three rehabilitated ponds to test whether the pond specifically designed for wildlife best supports avifauna.

2. Materials and Methods

2.1. Study Site Description and History

The site of the wastewater ponds is about 60 km southwest of the capital Doha and can be reached by Salwa Road (or, officially, Highway no. 5, Figure 1). The area is rural, with few nearby human settlements except for a small village 2 km north of the highway. Similar to the rest of Qatar (a subtropical desert), this area is characterized by a dry landscape receiving less than 80 mm annual precipitation. Summer temperatures often exceed 45 degrees Celsius, with high humidity. In the winter months, lower temperatures (around 15 degrees Celsius) are often associated with northerly winds and occasional sandstorms [21]. The flat expanse of compact sand and limestone rocks at the site is sparsely dotted with drought-tolerant shrubs, and there are notable human disturbances, such as off-road tracks (Figure 2). Before rehabilitation, at their peak size, the wastewater ponds occupied around 493 hectares (4.93 km2) of land and were sectioned off into several distinct ‘lagoon basins’, numbered from one to nine (Figure 3). Two surveys of bird diversity were taken before the rehabilitation (September 2015, December 2017) by independent contractors (detailed below). Rehabilitation began with the construction of a package treatment plant (PTP) that treats Al Karaana wastewater. In 2019, the pond basins were modified, either returned to their original desert habitat or turned into treatment sewage effluent (TSE) ponds, which directly receive the treated wastewater from the PTP (Figure 1 and Figure 3). Each of the TSE ponds was initially designed to serve a different purpose, such as hosting wildlife (TSE-1) or regulating overflow (TSE-3), which informed the design of their shape and size (Figure 3, Table S1).
At the time of the study, the TSE ponds collectively occupied 73 hectares, merely one-sixth of the original lagoon area. As part of the rehabilitation process, various plant species, including the common reed (Phragmites australis) and a camphorweed species (Pluchea dioscoridis), were introduced to help sustain wildlife [22]. Similarly, Nile tilapia (Oreochromis niloticus) were introduced as they can withstand high temperatures and reproduce in short spans of time [23]. TSE-1 had already been filled with water by the time we began surveys; TSE-2 reached its full depth in December 2019, at which point water started to enter TSE-3, the overflow pond. The water level in TSE-3 remained low (less than ~30 cm in the deepest part) for several months, fully evaporated in August and September of 2020, and then refilled. Since then, the waterflows have continued in TSE-3, which reached 2.8 m at its deepest part as of September 2022.

2.2. Survey Protocols

Field surveys were conducted over two years (December 2019–September 2021, using point count and line transects; a full overview of sampling dates is shown in Table S2). Birds were observed using 10× binoculars and a 20×–60× spotting scope and identified visually using field guides [24,25] and acoustically with an audio guide [26]. Species and number of individuals were recorded using the mobile app Counter [27]. Further, photographs were captured with a camera fitted with an 800 mm lens for later species identification in the case of birds that were not easily identifiable in the field. Because our primary goal was to compare diversity before and after rehabilitation, we concentrated sampling efforts in the months of September and December (when the pre-rehabilitation surveys had been conducted; see below). Additional time points were surveyed sporadically in order to examine how species diversity and individual abundance had changed following restoration and with the migratory season. Raw data on observations are available at http://doi.org/10.17632/dvg33yf3xr.1 (uploaded 2 September 2022). Taxonomy follows the IOC 11.2 naming conventions, and the Latin names for all species are in Tables S3–S5.
Each line transect survey followed a pre-set route along vantage points (VPs, see map in Figure 3). We followed the naming system of VPs used in the 2017 pre-study surveys. Survey time in the morning started between 0600 and 0700, following the 2017 report [23]. In the afternoons, the observations started around 1530 until sunset. Each of the surveys was about 4 to 5 h long. Routes differed for morning and evening surveys for best visibility against the sun (the detailed route is shown in the supplementary materials). Birds were counted along the entire route, spending as much or as little time necessary to fully count all individuals. All post-remediation surveys were done by K.-C.C., who was accompanied only once (9 December 2019) by two other observers, with records verified by K.-C.C.
For analyses relating to ecological niche and migratory status, we categorized species as being highly dependent on water or less dependent on water (i.e., terrestrial) using habitat assessments from [25] and as having been recorded as breeding in Qatar or not (Gavin Farnell, pers. comm.; see Tables S3 and S5 for categorizations).

2.3. Pre-Remediation Surveys

Before remediation, an ecological consulting firm [28] surveyed birds for three days and two nights in September 2015 (exact dates not reported). Only the presence of each species (not the abundance of individuals) was noted. A different consulting firm, KEO, surveyed bird diversity (noting both species presence and individual abundance) on 3 December 2017 from 11 different vantage points (Figure 3) [23]. For comparing diversity measures (see Section 2.4.1), we used only “shared” points from these pre-rehabilitation surveys (i.e., areas that became TSE ponds; VP1, -3, and -4 in 2017). The other areas (“not shared”) were restored as compact sandy desert, far from the wetlands (Figure 3). Note that the observers of the pre-remediation surveys were not the same persons as the post-remediation survey observers.

2.4. Statistical Analysis

2.4.1. Descriptive Statistics

The species richness in Al Karaana before (2015, 2017) and after (2019–2021) rehabilitation was calculated using Whittaker’s alpha, beta, and gamma diversity. Whittaker’s alpha diversity is the total number of species present in each period, while gamma diversity is the total number of species over both periods [29]. Beta diversity is the number of unique unshared species between periods [29]. Because we conducted more post-remediation surveys than there were pre-remediation surveys [23,28], we calculated these diversity measures on an arbitrarily chosen subset of dates, with a sample size equal to the pre-remediation surveys. The post-remediation dates were: 16, 25, and 30 September 2020 and 3, 17, and 24 September 2021 (morning surveys); 11 and 18 September 2020 and 2 and 16 September 2021 (afternoon surveys); 5 December 2019 and 2020 (Table S2).

2.4.2. Statistical Comparisons

For an overview of which data were used in which statistical comparisons, see Table S2. To compare diversity and incorporate relative species abundance, we compared Fisher’s alpha diversity between 2017 and 2019–2021 [30], calculated in R (R Development Core Team, Vienna, Austria) using the package vegan [31]. We compared the post-rehabilitation values of Fisher’s alpha to the single pre-rehabilitation value from 2017 using a two-tailed Wilcoxon test, treating each post-remediation December survey as an independent observation.
We evaluated how Fisher’s alpha changed over time after rehabilitation by fitting a linear model (i.e., ANOVA), including season (spring migration, summer, fall migration, or winter) and month of the study (with October 2019 set to 0), with observed alpha on each day as the response variable. September–November was considered the fall migration period, and February–May was considered the spring migration period (see the phenology of migration in the UAE; note that distinctions between over-wintering and migration periods can be difficult [20]). Residuals from the model were checked for normality by eye, as recommended by [32]. Building from this model, which considered values across the entire study site, we compared post-rehabilitation Fisher’s alpha levels across the three TSE ponds while controlling for season in a second linear model. For post-hoc comparisons of migratory stage effects, we examined t-tests for parameters after changing the reference level as needed.
To examine changes in the composition of the bird community, we used two approaches in the package vegan [31]: dendrograms based on Bray–Curtis dissimilarity indices and multi-dimensional scaling. We included both pre-and post-rehabilitation surveys for examining whole-site patterns. September 2015 pre-rehabilitation surveys were excluded because they reported only species presence, not abundance. We also used multi-dimensional scaling to explore differences in the bird community among TSE ponds post-rehabilitation. Because of strong seasonal effects (see results), we chose a priori to focus only on September data since this was the month with the highest between-year replication (Table S2). We examined how the abundance of each species changed between years depending on ecological niche and migratory status. For each month and year separately, we calculated the mean number of individuals per species. We then categorized each species as increasing or decreasing in abundance for each month based on the difference between means. We then used the direction of the abundance trend as a categorical response variable, with migratory status and habitat preference as categorical predictors, controlling for phylogenetic relatedness, in a Bayesian model using the package MCMCglmm [33]. We initially tested an interaction term between the two fixed effects, which we removed if it was not significant. We used recommended default uninformative priors (nu = 0.002, V = 1) with a burn-in of 1000 and thinning of 500, with 200,000 iterations [34]. The phylogeny was a consensus from 100 trees, with the Ericson backbone downloaded from birdtree.org. This approach is similar to [9]; however, since many observation periods included zero values, we were unable to log-transform in order to compare the magnitudes of abundance change. For simplicity, we created a separate model for each month since many species were observed only in a subset of months. To avoid having very rare observations influence the results, only species observed at least twice in the 2019–2021 study period were included. For comparisons at the level of the whole study site, we used data from all months where observations were made in two consecutive years: October, November, and December 2019; May, June, September, October, November, and December 2020; and May, June, and September 2021 (Table S2). To compare abundance trends across TSE ponds, only September data were available for two consecutive years, and we calculated abundance trends and constructed models separately for each pond.
To further compare TSE ponds, we compared how rapidly species accumulation curves increased over time using a Cox proportional hazard test in the package survival v.3.2–13 [35,36]. For this analysis, we included all observations made separately by TSE pond (i.e., July 2020–September 2021; Table S2).
Further, water quality data from each pool was obtained from the Arab Center for Engineering Studies and Metito through Ashghal, the Qatar Public Works Authority, to analyze, among other parameters, dissolved oxygen, chemical oxygen demand, biochemical oxygen demand, and ammonia levels.

3. Results

3.1. Comparison before and after Rehabilitation

Between 2019 and 2021, in all observations (including most calendar months), we observed 96 species and 21,998 individuals during formal surveys; three species were observed just outside the survey area (see data supplement at http://doi.org/10.17632/dvg33yf3xr.1) (uploaded 2 September 2022). Forty-four of these species had also been observed in shared areas in the pre-rehabilitation surveys. Whittaker’s alpha diversity after remediation was higher than before remediation for both September and December (Table 1). The beta diversity between the months of September of different years was higher than that of the months of December (Table 2). Similarly, the gamma diversity of September 2015, 2020, and 2021 was more than that of December 2017, 2019, and 2020 (Table 2).
Fisher’s alpha was significantly higher in December after rehabilitation (mean 7.60) than before rehabilitation (value of 2.85 from the single observation day in December 2017; Wilcoxon V = 21, p = 0.03, df = 5). We could not compare Fisher’s alpha for September because the pre-rehabilitation data did not include individual counts.
Examining the results from two arbitrarily chosen days before and after remediation showed that the most abundant species (i.e., species with the highest number observed) in both December 2017 and December 2020 was the Little Stint (Calidris minuta, Table 3).
The total number of species observed in the months of September and December (all years) was 85. Out of the 85 species, only 5 species were present in all six observations (September and December of three years each): Black-winged Stilt (Himantopus himantopus), Common Sandpiper (Actitis hypoleucos), Grey Heron (Ardea cinerea), Little Grebe (Tachybaptus ruficollis), and Little Stint (Calidris minuta).

3.2. Impact of Migrants and Over-Wintering Birds on the Bird Community

Observations from September and December each clustered strongly together, and data from different years formed sub-clusters within each month (Figure 4). Shared vantage points from 2017 (pre-rehabilitation) were more similar to the 2019 and 2020 data than unshared vantage points, albeit with a long arm between the clusters. In a clustering analysis that included the 2015 data but did not use abundance (only presence–absence), patterns were largely similar, except that the December 2017 data were basal to all other groups, and the separation between post-rehabilitation years within months was less clear (not shown).
There was no overall trend in Fisher’s alpha diversity between October 2019 and September 2021 (Figure 5; F1,48 = 0.86, p = 0.36). However, season had a significant effect (F3,48 = 3.61, p = 0.02). Post-hoc comparisons of parameter estimates showed that diversity was higher in winter than in spring or summer (|t48| > 2.1, p < 0.05), and fall tended to be more diverse than summer (t48= −1.87, p = 0.07), with other comparisons being not significant (all |t48| < 1.7, p > 0.10; note that spring is represented by only 3 observation days). Differences in the bird community across the year were also apparent (Figure 6), with the community showing gradual changes across months, which were roughly parallel between years, although the years also differed somewhat.

3.3. Change in the Site following Rehabilitation: Whole Site

Similar numbers of species were increasing in abundance or decreasing in abundance for each of the six months observed in two consecutive years (Table 4 and Table S3; additional species observed too infrequently to be included in the analyses are in Table S4). We found no evidence that either breeding status or habitat preference (or their interaction) was related to whether species were increasing or decreasing in abundance (Figure 7, all p > 0.06 before correction for multiple testing; models also controlled for phylogeny, effective sampling size from Bayesian models all > 59; sample sizes in Table 4). These changes were also reflected as changes in bird community composition between years (Figure 4).

3.4. Change in the Site following Rehabilitation: Comparing TSE Ponds

In water quality tests conducted from 2020 to 2021, a gradual increase in pH is seen in TSE-1, with the highest value (9.46) observed in August 2021. A similar increase is observed in TSE-2 from 2020 to 2021. Though there was no 2020 pH reading for TSE-3 due to its drying out, its pH in August 2021 was alkaline as well (8.97; Table S6). Vegetation growth was observed throughout the study. As of the end of the study (September 2021), reeds had completely surrounded TSE-1 and TSE-2 and extended to the northeastern edge of TSE-3 (see Figures S4 and S5).
Salinity levels ranged between 0.5 and 38 ppt (Figure 8). The salinity levels of TSE-3 were consistently higher than both TSE1 and TSE2, which had similar levels.
Neither breeding status nor habitat preference was significantly related to whether the species was increasing or decreasing in abundance within each TSE pond when controlling for phylogeny (Figure 9, Table S5, all p > 0.1, all Bayesian effective sample sizes > 11; n = 55 species for TSE-1; 44 species for TSE-2; 53 species for TSE-3). Differences in the bird communities between years for each TSE pond and among TSE ponds are apparent following multi-dimensional scaling (Figure 10).
Despite the initially slow habitat development of TSE-3 compared to TSE-1 and TSE-2, the bird species accumulated at statistically similar rates in all three pools (chi-squared test = 2.57, df = 2, p = 0.28; Figure 11).
When controlling for the significant effect of season (see whole-site results), we also found a significant difference in Fisher’s alpha among TSE ponds (F2,93 = 3.39, p = 0.04). Post-hoc testing showed that TSE-2 had lower diversity than TSE-1 (t = −2.59, p = 0.01), while TSE-3 did not differ from either TSE-1 or TSE-2 (both |t| < 1.5, p > 0.13; Figure 12).

4. Discussion

Our observations indicate that, as of September 2021, Al Karaana Lagoons support a thriving ecosystem with high bird diversity. From 2015 to 2021, records of total avian species showed a marked increase, along with Whittaker’s alpha, beta, and gamma diversity values before and after remediation. The avian biodiversity has seen significant improvement following the environmental remediation, with a population composed of both resident and migratory species.

4.1. Changes in the Bird Community following Rehabilitation

Comparing bird presence pre- and post-rehabilitation of Al Karaana Lagoons, an overall increase in Fisher’s alpha diversity index showed improvement in biodiversity with remediation. Therefore, our results support previous studies showing that the bird community can recover quickly following wetland restoration [4,18]. Fisher’s alpha index specifically allows for comparisons to be made between different sites [37], so our results imply that species diversity is likely improving throughout the entire site, though perhaps to a lesser degree for TSE-2 than the other TSE ponds. Further, an increase in Whittaker’s alpha diversity indicates an increase in the number of unique bird species after remediation. Changes in the composition of the bird community over the years—visualized in Figure 5 and Figure 9—point toward some turnover in the species inhabiting the wetlands over time after remediation. It has previously been noted that species and foraging guilds can differ in how they respond to wetland restoration [9], although we did not find evidence that broad ecological preferences (primarily terrestrial or aquatic) affected whether individual species were increasing or decreasing in abundance. This increased bird diversity and the changes in community composition may be due to improved water quality (unfortunately, pre-remediation data on water quality are limited, so we cannot provide a thorough test) as well as the improved physical characteristics of the TSE ponds compared to the lagoons prior to remediation (see Section 4.2). Supporting this interpretation, the abundance of individuals and the diversity of bird species are known to be negatively impacted by pollutants in other contexts (e.g., heavy metal pollution from smelting [38]; electronic waste from recycling centers [39]; agricultural chemicals [40]; urban air pollution [41]). Unfortunately, the pre- and post-remediation surveys were conducted by different observers, which may add error to the pre- and post-remediation comparison. However, given the magnitude of the improvement in diversity (post-rehabilitation diversity was approximately twice the diversity pre-rehabilitation), we suspect that error due to observer differences is unlikely to fully explain the improvements.
Individual abundances of different species showed varying patterns following rehabilitation; previous studies also showed substantial heterogeneity in how individual species respond to wetland restoration (e.g., [9,18]) and environmental pollutants [39]. Along with the increase in diversity with regard to birdlife, an increase in the diversity of vegetation and microorganisms is highly likely according to the water quality tests (Table S6). As indicated by the high nutrient levels, such as that of ammonia, TSE-1 water can be classified as eutrophic [42]. Despite a few fluctuations in ammonia, measured as its nitrogen content (NH3 as N), data from 2020 to 2021 showed a general increase in both TSE-1 and TSE-2. In addition, the observed high values of COD and BOD indicate an oxygen deficit in the water of Al Karaana Lagoons [43], which is likely a direct result of this eutrophication, leading to oxygen deprivation that is unfavorable for supporting fish life, which, in turn, impacts piscivorous birds. Turbidity in the water due to eutrophication has also been linked to a lower abundance of some water birds, perhaps because it diminishes foraging efficiency [44]. It is acknowledged, however, that different bodies of water handle nutrient enrichment differently, and thus, it is difficult to predict what levels will cause adverse effects [45,46]. Conversely, it has also been suggested that eutrophication can improve the habitat for some bird species or, at least, correlates with high wetland primary productivity rates that support more biomass at higher trophic levels [45,47], which may help explain the high bird biodiversity observed at Al Karaana Lagoons. Both natural and constructed wetlands are generally known to control nutrient concentrations to levels that can support all wildlife of the ecosystem [48]. Effects of eutrophication are further apparent in the gradual increase in pH over time. This pattern can be explained by ongoing eutrophication, resulting in bloom-induced basification [49]. High alkalinity can potentially be harmful to aquatic life, so monitoring pH is of extreme importance. Having said that, the buffering capability of alkaline bodies of water is intrinsic to the protection of aquatic life against pH changes [43] and may, therefore, be a factor contributing to Al Karaana Lagoons’ increased biodiversity. For example, the abundance of the Little Grebe (Tachybaptus ruficollis) in a lake in Pakistan was higher in periods with higher alkalinity, indicating that high pH may not necessarily immediately reduce bird populations [44]. We do not have access to detailed information on water quality before remediation, making it difficult to ascertain how dramatically the water quality has changed.
Water nutrient levels directly impact the growth of algae that are food for macroinvertebrates, which, in turn, are major food sources for aquatic birds. The nutrient levels may, on one hand, affect the emergent vegetation (i.e., reeds) growing along the edges of the ponds as well as in the shallow areas [39]; the nutrient levels may also be stabilized by the presence of these macrophytes [50]. While emergent vegetation can provide an important habitat for both birds and their prey, vegetation that is too dense or too tall may be detrimental to birds’ foraging success [51].

4.2. Comparison of Different TSE Pond Designs

Wetland restoration efforts may take a variety of approaches (e.g., re-vegetating or not) in order to best recreate the original wetland habitat, and the restoration approach does not strongly predict the effectiveness of the restoration [5]. At Al Karaana Lagoons, the design of each of the three pools was tailored to a specific purpose. For instance, there were intentional introductions of alien plants (e.g., Phragmites australis) and fish (e.g., Oreochromis spp.) species in TSE-1 to serve as shelter and food for wildlife to promote biodiversity in the pond [23]. On the other hand, TSE-3 was constructed with the specific purpose of managing overflow and allowing evaporation. These differences are reflected in certain qualities of the pools, such as salinity and depth profiles, as well as in the consistent differences in the bird communities they support. Water salinity can affect the diversity of vegetation that can grow at or around the ponds, which then indirectly affects the diversity of herbivorous bird populations that are present. Several “high quality” plants for waterbirds grow better in lagoons with mildly brackish water, with salinity values around 2–7 ppt [51]. For this reason, many herbivorous waterbirds prefer ponds with lower salinities to acquire food of higher quality. TSE-1 and TSE-2 are at similar salinity levels, with TSE-2 being slightly more saline despite a smaller surface area due to its longer exposure to evaporation. TSE-3 consistently has a much higher salinity level compared to TSE-1 and TSE-2; this is likely due to the fact that TSE-3 has gone through the longest exposure to evaporation. TSE-3 has the greatest surface area, making the water highly susceptible to evaporation; it is usually the smallest water body, despite having the largest capacity of the three TSE ponds, as it is the furthest away from the only water outlet from the PTP to the TSE ponds. The high salinity of TSE-3 provides a less-than-ideal environment for most freshwater organisms. It is plausible that TSE-3 could increase in salinity over time and, as a result, become a lower-quality habitat for bird species that rely on freshwater prey. However, it is worth noting that during the summer of 2020, prior to the complete evaporation of TSE-3, when the salinity reached 38 ppt, we observed an abundant number of waders, mostly Little Stints (Calidris minuta), actively foraging in the shallow water and through the cracked substrates. Therefore, although high salinity may impact sensitive macroinvertebrates, salt-tolerant species, including mollusks and larvae of Coleoptera, may be less affected [39] and continue to serve as a food supply for these birds.
The depth profiles of the ponds also appear to impact bird diversity, as observed in prior studies on wetlands (e.g., [8]). Water depth is an important factor affecting the biodiversity of birds due to its effects on foraging [51]. Even with the same food abundance in a body of water, many waterbirds are able to acquire more net energy intake from shallower areas, likely because shallow waters generally make it easier for waterbirds to find and catch prey or reach submerged vegetation, depending on the diet. The density and diversity of waterbirds are usually elevated in shallower water depths, where depth requirements of waterbirds with different foraging strategies (e.g., dabbling and wading) overlap, such as 10–20 cm [51]. The combination of emergent vegetation, providing shelter to birds, and open water where diving birds can hunt has been noted as promoting birdlife in previous studies [44]. TSE-2 was not built specifically to provide a habitat, so it has a simple physical structure, being steep-sided and deep, without a shallow area for wading species, leading to it having lower avian diversity than the other ponds. Consistent with this simple structure, only species of waterbirds that breed in Qatar have substantially increased in abundance in this pond (note that the annual abundance of migratory species can be highly variable among years, which would add noise to this two-year dataset; [19]). With a depth of 5 m, TSE-2 may be deep enough that foraging could be less than optimally efficient for diving birds compared to a somewhat shallower pool [51]. However, despite not being built specifically for it, TSE-2 supports substantial aquatic life, vegetation, and bird life. In contrast to TSE-2, TSE-1 was designed to have a shallow area and small islets to accommodate bird diversity, and TSE-3 currently has a shallow area because of how overflow from TSE-2 enters this pond. These shallow areas may explain the higher diversity of these two ponds as well as how they are inhabited by more similar bird communities compared to TSE-2 (Figure 10). Additionally, there has been a longer period of adjustment to better accommodate aquatic life in TSE-1 as it was the first pond where remediation was completed, promoting diversity. Thus, the construction of TSE-1, with a bird habitat in mind, appears to have been successful (see also [51]). The water level at TSE-3 may also be expected to fluctuate more than the other TSE ponds due to its much greater surface area. Thus, it is key to note that if fluctuations are sufficiently large, any nests built close to the water level may be subject to flooding, creating a situation where TSE-3 could represent an ecological trap [51]. The abundance of breeding birds, in particular, can fluctuate quickly in response to local conditions (e.g., [50]).

4.3. Importance for Migratory Species

Given the location of Al Karaana Lagoons on the African–Eurasian flyway, their avian biodiversity is highly dependent on visiting migratory species. Unsurprisingly, bird diversity (Fisher’s alpha) was higher in the migratory and over-wintering periods compared to the summer, and changes in the avian community over the annual cycle were apparent, with the bird community composition showing a gradient across the season between summer and winter. Higher diversity in the fall and winter may have been driven by the second observation season (Figure 5), perhaps because more time had elapsed, during which the ecosystem may have become more complex and developed. Because our surveys focused primarily on fall and winter, to maximize comparability of pre- and post-rehabilitation diversity, our surveys may have missed some species that primarily stop over on the eastern Arabian Peninsula in the spring migration but not the fall migration (including predominantly passerine species: [20]). Differences between the spring and autumn migrations in the Arabian Peninsula have been well documented (e.g., [52]). The patterns of Whittaker’s alpha, beta, and gamma diversity and Fisher’s alpha are consistent with an influx of passage migrants in September as well as over-wintering species, which depart for breeding grounds before the summer. There is a clear decrease in Whittaker’s alpha, beta, and gamma diversity values from September to December, likely due to the presence of passage migrants in September but not December. Beta diversity was relatively high between years in September, indicating that a substantial number of species was observed only in one year in this month. September may include passage migrants, which may be present in lower numbers and/or be more difficult to detect, which may help explain the high beta diversity. Lower beta diversity for December indicates fewer unique species observations in different years for this month. Species still present in December are likely to be over-wintering and could be more reliably detected. Similarly, the gamma diversity is higher in the months of September compared to the months of December. As gamma diversity highlights the total abundance of bird species over a period, September is considered more diverse than December.
Seasonal differences in the assemblage of birds were also evident from clustering analyses, which showed greater similarity among observations taken in the same month than among observations taken in the same year. Across all sampling months, a gradient appeared, showing that the community of birds gradually changes, likely due to the migratory cycle. The seasonal patterns in the bird community are further highlighted by the stronger similarity of the December (over-wintering) pre-restoration data to the December post-restoration data compared to the September (fall migration) post-restoration data. The species of birds visiting the site during the migratory season remain similar pre- and post-restoration and across the two post-restoration years.
The method used in counting the species does not account for possible detection bias across days or seasons. For example, there are more windy days during winter than during fall, which might result in the underestimation of the number and abundance of bird species detected during the winter season. Other factors affecting detection probability include observer experience as well as survey timing, which requires knowledge of each species’ biological cycle in order to optimize sightings [53]. In addition to the species seen during the formal observation periods, additional species were seen anecdotally. For example, a Steppe Eagle (Aquila nipalensis) was observed near TSE-2, and a Little Owl (Athene noctua) was observed just beyond the main study area on many of the field visits. These observations highlight the potential for Al Karaana Lagoons to harbor substantial avian biodiversity.

4.4. Management and Future Prospects

Noting the role of Al Karaana Lagoons as a hub of avian wildlife, the protection of bird species in the area, going forward, is important to maintaining and promoting bird biodiversity. While most of the observed species are classified as “least concern” according to International Union for Conservation of Nature (IUCN), several are “near threatened” (Black-tailed Godwit, Limosa limosa) or “vulnerable” (Common Pochard, Aythya ferina, and Great Grey Shrike, Lanius excubitor), highlighting the potential importance of this site for bird conservation. Several other artificial wetlands and other human-created landscapes, such as large agricultural areas that rely on irrigation to support plant growth, exist in Qatar. Al Karaana Lagoons may therefore be viewed as one set of wetlands within a mosaic landscape, separated by substantial arid zones from other relatively highly vegetated areas. Connectivity among these human-created landscapes may help increase the total bird diversity observed at Al Karaana Lagoons as well as in Qatar in general.
One important aspect of preserving this restored wetland will be to balance the needs of human visitors and birdlife. Allowing people access to the site appears important as there are relatively few comparable areas of semi-wilderness in Qatar, and interacting with nature may be an important factor in encouraging people to learn about nature and conserve it. However, in order to promote the safety and breeding success of the birds, we suggest that a number of limits be placed on human use of the wetland. For example, currently, the discharge of firearms is common at the field site (apparently for recreational purposes; pers. obs.), as well as rapid off-road driving with loud racing engines. These activities not only damage the physical structures, i.e., the slopes of the shores and the bunds, increasing the rate of sediment deposits to the ponds, but they appear to cause substantial disturbance to the birds (see also [8]). This disturbance may partly explain why several relatively shy species, such as Greater Flamingoes (Phoenicopterus roseus) and Black-winged Stilts (Himantopus himantopus), have become somewhat less common over time. In addition to reducing firearm use and rapid driving, we recommend procedures that have been successful in other areas, such as limiting the number of days the site is open to the public and which portions of the site are accessible [54,55].
In addition to regulating human use, we recommend continued monitoring and, as much as possible, the regulation of water quality and plant life at Al Karaana Lagoons. Salinity, water level fluctuations, eutrophication, and the density of the emergent vegetation may all affect the bird community, as indicated above [51]. While it may not be feasible to regulate salinity and water levels in TSE-3 while still achieving the main water purification functions of Al Karaana Lagoons, it may be possible to regulate the density of the emergent vegetation to some extent. For example, controlled burns have previously been used to reduce the density of vegetation to support birds [51,56]. Seasonal harvest of Phragmites australis has the potential to further regulate the eutrophic state of TSE pond water [57]. Whether such a strategy could or should be implemented at Al Karaana Lagoons would require further studies.

5. Conclusions

This study indicates a significant increase in post-remediation bird diversity at Al Karaana Lagoons. Qatar has the potential to play an important role as a stopover site for migratory species, both at the Al Karaana Lagoons and in other types of habitats (e.g., urban parks: [19], intertidal mudflats: [58], coastal mangroves: [59]). The success of protected areas in the Arabian Peninsula at providing a habitat to migratory and resident birds has been noted in other studies [52,54,55]. Monitoring birds in Qatar is, therefore, important, both for understanding the population trends of migratory species in the country as well as for human health, given the potential for migratory birds to carry diseases and disease vectors (e.g., [60]).

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/birds3040022/s1, Table S1: Characteristics of TSE ponds as displayed at the Al Karaana wetland (Ashghal, Qatar Public Works Authority); Table S2: Overview of sampling dates, whether data were recorded separately for each TSE pond, and which analyses the observation dates were included with; Table S3: Number of individuals and changes in abundance, comparing averages from two consecutive years, within months; Table S4: Additional species observed infrequently enough that they were not included in the comparison of abundances; Table S5: Number of individuals and changes in abundance, comparing averages from September 2020 and September 2021, for three different TSE ponds; Table S6: Compilation of various water quality tests conducted from 2020–2021; Figure S1: Pre-remediation observation of oil slick at “Vantage Point 2” in the 2015 report; Figure S2: Pre-remediation observation of surface contamination in the southern region of the former Lagoon 3 (L3), which is currently TSE-3 (see Figure 2 of main text); Figure S3: Post-remediation observation of the southwestern corner of TSE-3, same location as the former southern region of the L3 in Figure S2; Figure S4: Post-remediation aerial view of TSE-1 pond, foreground, TSE-2 and TSE-3 ponds, upper-right looking southeastward; Figure S5: Post-remediation aerial view of TSE-2 pond, foreground and TSE-3 pond, background looking southeastward.

Author Contributions

Conceptualization, K.-C.C. and E.R.A.C.; methodology, K.-C.C.; formal analysis, E.R.A.C., M.T. and A.D.; writing—original draft preparation, A.D., M.T. and N.B.; writing—review and editing, K.-C.C. and E.R.A.C.; supervision K.-C.C. and E.R.A.C.; funding acquisition, K.-C.C., A.D. and M.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Student Research Mentorship Program (SRMP 004-03) from Weill Cornell Medicine-Qatar in 2021.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data are publicly available at Mendeley Data (http://doi.org/10.17632/dvg33yf3xr.2) (accessed on 2 September 2022).

Acknowledgments

The authors thank Ashghal, the Qatar Public Works Authority, for permitting access to the study sites and providing water quality reports and the pre-remediation ecological survey reports. We thank Gavin Farnell for the verification of some bird species. Lastly, we thank three anonymous reviewers provided their comments to improve our original manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Satellite photos showing the Al Karaana Lagoons area, obtained from Google Earth and Google Earth’s timelapse function: top, showing the geographic location of the Al Karaana Lagoon area (red pin, September 2022, scale bar 600 km); bottom, set of six photos showing the relatively undisturbed state in 2000–2005, the full extent of the area for untreated waste in 2013 and 2015, rehabilitation in progress in 2019, and after rehabilitation in 2020 (scale bar 2000 m). In lower panels labeled with the year, white to tan colors are the compact sandy desert habitat. Dark colors are water, either untreated wastewater (before 2019) or treated wastewater (2020). The road lying north and west of the study site is Salwa Road or Highway no. 5.
Figure 1. Satellite photos showing the Al Karaana Lagoons area, obtained from Google Earth and Google Earth’s timelapse function: top, showing the geographic location of the Al Karaana Lagoon area (red pin, September 2022, scale bar 600 km); bottom, set of six photos showing the relatively undisturbed state in 2000–2005, the full extent of the area for untreated waste in 2013 and 2015, rehabilitation in progress in 2019, and after rehabilitation in 2020 (scale bar 2000 m). In lower panels labeled with the year, white to tan colors are the compact sandy desert habitat. Dark colors are water, either untreated wastewater (before 2019) or treated wastewater (2020). The road lying north and west of the study site is Salwa Road or Highway no. 5.
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Figure 2. Disturbed limestone gravel plain by tire tracks and used tires as the typical landscape at the Karaana study site.
Figure 2. Disturbed limestone gravel plain by tire tracks and used tires as the typical landscape at the Karaana study site.
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Figure 3. Map of Al Karaana Lagoons project area. L1a through L8 are the names of the former wastewater ponds. All but part of L3 and L5 have been restored back to their original state of compact sandy soil. Treated sewage effluent pond (TSE)-1 is located in a part of the original L5 basin, while TSE-2 and TSE-3 are situated in the former L3. The teal blue and dark blue areas represent the TSE ponds post-remediation, with greater depth indicated by the dark blue. Pre-remediation (2017) survey vantage points (VPs) are also marked. The package treatment plant (PTP), where the water is purified, is shown on the right. TSE-1 has a shallow area; TSE-2 has relatively steep sides with no shallow areas; TSE-3 has a shallow area by the inlet on the eastern side, while the greatest depth is located in the southern end (Table S1). As of the end of the study (September 2021), reeds have completely surrounded TSE-1 and TSE-2 and extended to the northeastern edge of TSE-3. At the conclusion of this field study, L9 continued to receive petroleum waste into the lined basins, awaiting the completion of a new industrial waste treatment plant located elsewhere before this basin is sealed (pers. comm. with Ashghal).
Figure 3. Map of Al Karaana Lagoons project area. L1a through L8 are the names of the former wastewater ponds. All but part of L3 and L5 have been restored back to their original state of compact sandy soil. Treated sewage effluent pond (TSE)-1 is located in a part of the original L5 basin, while TSE-2 and TSE-3 are situated in the former L3. The teal blue and dark blue areas represent the TSE ponds post-remediation, with greater depth indicated by the dark blue. Pre-remediation (2017) survey vantage points (VPs) are also marked. The package treatment plant (PTP), where the water is purified, is shown on the right. TSE-1 has a shallow area; TSE-2 has relatively steep sides with no shallow areas; TSE-3 has a shallow area by the inlet on the eastern side, while the greatest depth is located in the southern end (Table S1). As of the end of the study (September 2021), reeds have completely surrounded TSE-1 and TSE-2 and extended to the northeastern edge of TSE-3. At the conclusion of this field study, L9 continued to receive petroleum waste into the lined basins, awaiting the completion of a new industrial waste treatment plant located elsewhere before this basin is sealed (pers. comm. with Ashghal).
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Figure 4. Bird community similarity in September (Sep, red) and December (Dec, blue) before restoration work (dashed lines) and after restoration (solid lines) at Al Karaana Lagoons in Qatar. Note that the period after restoration includes two years. Abundance data for each observed species were used.
Figure 4. Bird community similarity in September (Sep, red) and December (Dec, blue) before restoration work (dashed lines) and after restoration (solid lines) at Al Karaana Lagoons in Qatar. Note that the period after restoration includes two years. Abundance data for each observed species were used.
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Figure 5. Fisher’s alpha diversity index over time. Background shading and boxplot colors indicate stages in the annual cycle (dark grey shading, over-wintering; light grey shading, migration; green boxplots, summer; yellow box plots, fall; orange boxplots, winter; blue boxplots, spring). Boxplots show the median and interquartile range; whiskers include all observations within 1.5 x IQR (interquartile range), and outliers are represented by points.
Figure 5. Fisher’s alpha diversity index over time. Background shading and boxplot colors indicate stages in the annual cycle (dark grey shading, over-wintering; light grey shading, migration; green boxplots, summer; yellow box plots, fall; orange boxplots, winter; blue boxplots, spring). Boxplots show the median and interquartile range; whiskers include all observations within 1.5 x IQR (interquartile range), and outliers are represented by points.
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Figure 6. Changes in the composition of the bird community over time. Colors show different months, and symbol shapes reflect years. Each point represents one day’s observations (2017 data include both the shared and unshared vantage points combined).
Figure 6. Changes in the composition of the bird community over time. Colors show different months, and symbol shapes reflect years. Each point represents one day’s observations (2017 data include both the shared and unshared vantage points combined).
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Figure 7. Number of species with increasing (blue) or decreasing (red) abundance of individuals, depending on whether the species is primarily aquatic or terrestrial and whether the species breeds in Qatar. Only species seen at least twice on the site were included. Each panel represents a different month; comparisons were between consecutive years (see Table 4).
Figure 7. Number of species with increasing (blue) or decreasing (red) abundance of individuals, depending on whether the species is primarily aquatic or terrestrial and whether the species breeds in Qatar. Only species seen at least twice on the site were included. Each panel represents a different month; comparisons were between consecutive years (see Table 4).
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Figure 8. Collected salinity level readings of treated sewage effluent ponds (TSE) -1, -2, and -3. The water in TSE-3 completely evaporated in the summer of 2020 before refilling in the fall of that year. Prior to full evaporation, its salinity reached 38 ppt. TSE-1 and TSE-2 were filled to capacity the entire study period. Since refilling began in TSE-3 in September 2020, the salinity in all three ponds has been mostly maintained below 4 ppt.
Figure 8. Collected salinity level readings of treated sewage effluent ponds (TSE) -1, -2, and -3. The water in TSE-3 completely evaporated in the summer of 2020 before refilling in the fall of that year. Prior to full evaporation, its salinity reached 38 ppt. TSE-1 and TSE-2 were filled to capacity the entire study period. Since refilling began in TSE-3 in September 2020, the salinity in all three ponds has been mostly maintained below 4 ppt.
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Figure 9. Number of species with increasing (blue) or decreasing (red) abundance of individuals, depending on whether the species is primarily aquatic or terrestrial and whether the species breeds in Qatar. Only species seen at least twice on the site were included. Each treated sewage effluent pond (TSE) is in a different pair of panels. Data are from September 2020 and September 2021.
Figure 9. Number of species with increasing (blue) or decreasing (red) abundance of individuals, depending on whether the species is primarily aquatic or terrestrial and whether the species breeds in Qatar. Only species seen at least twice on the site were included. Each treated sewage effluent pond (TSE) is in a different pair of panels. Data are from September 2020 and September 2021.
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Figure 10. Changes in the composition of the bird community in September between 2020 and 2021 (symbol shape) and among the three treated sewage effluent ponds (TSE; colors). Each point represents one day’s observations.
Figure 10. Changes in the composition of the bird community in September between 2020 and 2021 (symbol shape) and among the three treated sewage effluent ponds (TSE; colors). Each point represents one day’s observations.
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Figure 11. Species accumulation curves showing the cumulative number of species observed over time after rehabilitation for each treated sewage effluent pond (TSE; July 2020 = month 0). TSE ponds did not differ significantly in how quickly species accumulated (chi-squared = 2.57, df = 2, p = 0.28). The line shows when new species were observed, and the shading indicates 95% confidence intervals around observation time.
Figure 11. Species accumulation curves showing the cumulative number of species observed over time after rehabilitation for each treated sewage effluent pond (TSE; July 2020 = month 0). TSE ponds did not differ significantly in how quickly species accumulated (chi-squared = 2.57, df = 2, p = 0.28). The line shows when new species were observed, and the shading indicates 95% confidence intervals around observation time.
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Figure 12. Fisher’s alpha diversity index over time after wetland rehabilitation at each treated sewage effluent pond (TSE) separately. Background shading and boxplot colors indicate stages in the annual cycle (dark grey shading, over-wintering; light grey shading, migration; green boxplots, summer; yellow box plots, fall; orange boxplots, winter; blue boxplots, spring). Boxplots show the median and interquartile range; whiskers include all observations within 1.5 x IQR (interquartile range), and outliers are represented by points. Each TSE pond is in a different panel.
Figure 12. Fisher’s alpha diversity index over time after wetland rehabilitation at each treated sewage effluent pond (TSE) separately. Background shading and boxplot colors indicate stages in the annual cycle (dark grey shading, over-wintering; light grey shading, migration; green boxplots, summer; yellow box plots, fall; orange boxplots, winter; blue boxplots, spring). Boxplots show the median and interquartile range; whiskers include all observations within 1.5 x IQR (interquartile range), and outliers are represented by points. Each TSE pond is in a different panel.
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Table
Table 1. Comparison of Whittaker’s alpha diversity calculated before and after remediation; note that there are two post-remediation years for each month.
Table 1. Comparison of Whittaker’s alpha diversity calculated before and after remediation; note that there are two post-remediation years for each month.
Time PeriodWhittaker’s Alpha Diversity
Whittaker’s Alpha DiversitySeptember (Year)December (Year)
Before remediation31 (2015)18 (2017)
After remediation53 (2020), 50 (2021)32 (2019), 31 (2020)
Table
Table 2. Comparison of beta and gamma diversity in September and December before and after remediation.
Table 2. Comparison of beta and gamma diversity in September and December before and after remediation.
Months Before and After Remediation, RespectivelyBeta DiversityGamma Diversity
September 2015 vs. September 20203469
September 2015 vs. September 20213960
September 2020 vs. September 20213971
December 2017 vs. December 20192437
December 2017 vs. December 20202537
December 2019 vs. December 20202864
Table
Table 3. Preliminary observation of arbitrary sampling in December 2017 and December 2020.
Table 3. Preliminary observation of arbitrary sampling in December 2017 and December 2020.
Total No. of Avian IndividualsMost Abundant SpeciesNumber of Individuals from the Most Abundant Species
Before remediation (3 December 2017)863Little Stint
(Calidris minuta)		300
After remediation (5 December 2020)1011Little Stint
(Calidris minuta)		116
Table
Table 4. Number of species increasing or decreasing in abundance between consecutive years. Only species observed at least twice in the study (2019–2021) were considered to minimize the impact of rare observations.
Table 4. Number of species increasing or decreasing in abundance between consecutive years. Only species observed at least twice in the study (2019–2021) were considered to minimize the impact of rare observations.
MonthYears ComparedN species IncreasingN species Decreasing
May2020–2021173
June2020–20211318
September2020–20213136
October2019–20202018
November2019–20203216
December2019–20202930
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MDPI and ACS Style

Draidia, A.; Tareen, M.; Bayraktar, N.; Cramer, E.R.A.; Chen, K.-C. Bird Communities and the Rehabilitation of Al Karaana Lagoons in Qatar. Birds 2022, 3, 320-340. https://doi.org/10.3390/birds3040022

AMA Style

Draidia A, Tareen M, Bayraktar N, Cramer ERA, Chen K-C. Bird Communities and the Rehabilitation of Al Karaana Lagoons in Qatar. Birds. 2022; 3(4):320-340. https://doi.org/10.3390/birds3040022

Chicago/Turabian Style

Draidia, Ayaterahman, Momina Tareen, Nuran Bayraktar, Emily R. A. Cramer, and Kuei-Chiu Chen. 2022. "Bird Communities and the Rehabilitation of Al Karaana Lagoons in Qatar" Birds 3, no. 4: 320-340. https://doi.org/10.3390/birds3040022

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