ORI GIN AL PA PER

Shorebird assemblages respond to anthropogenic stressby altering habitat use in a wetland in India

K. M. Aarif • S. B. Muzaffar • S. Babu • P. K. Prasadan

Received: 7 August 2013 / Revised: 9 January 2014 / Accepted: 15 January 2014� Springer Science+Business Media Dordrecht 2014

Abstract Shorebirds are globally experiencing declines due to habitat loss and anthro-

pogenic disturbance. The Central Asian Flyway hosts significant shorebirds that winter in

the Indian subcontinent. The current study examined the shorebird assemblages of Ka-

dalundi-Vallikkunnu Community Reserve, an internationally important estuarine wetland

in southwestern India, to determine changes in their assemblages in relation to habitat

alterations. We conducted point counts from 2005 to 2012 in mudflats, mangroves, sandy

beaches and shallow water areas in Kadalundi-Vallikkunnu Community Reserve. This

study measured physicochemical variables as a proxy for anthropogenic change experi-

enced as a result of rapidly increasing human populations combined with development. We

examined rainfall data during the study period to determine associations with shorebird

abundance. Stepwise linear regression showed that total nitrogen and rainfall were sig-

nificantly related to shorebird abundance (bird count = 306 ? 213 NO3-—1.13 rainfall,

F = 31.20, p \ 0.001). High rainfall in a given year (one-way ANOVA F = 19.91,

p \ 0.001) and the previous year resulted in lower shorebird counts (one-way ANOVA

Communicated by Stephen Garnett.

K. M. Aarif � P. K. PrasadanResearch Department of Zoology, Mary Matha Arts and Science College, Mananthavady, Vemom PO,Wayanad District, Kerala, Indiae-mail: achuarif@gmail.com

P. K. Prasadane-mail: pkprasadan@gmail.com

S. B. Muzaffar (&)Department of Biology, United Arab Emirates University, PO Box 15551, Al Ain, United ArabEmiratese-mail: s_muzaffar@uaeu.ac.ae

S. BabuOrnithology Division, Salim Ali Centre for Ornithology and Natural History, Anaikatty (PO),Coimbatore 641 108, Tamil Nadu, Indiae-mail: sanbabs@gmail.com

123

Biodivers ConservDOI 10.1007/s10531-014-0630-9

F = 16.01, p \ 0.001). Shorebirds declined during the study period and habitat use shifted

significantly from mangroves and mudflats to sandy beaches (one-way ANOVA, F = 2.18,

p = 0.034). Shorebirds also exhibited a gradual decline in diversity. We conclude that

altered nutrient content in this wetland resulted in changes in the prey base in the four

habitat types. Shorebirds responded to these changes by increasing the use of less preferred

habitat (sandy beaches). The anthropogenic influences on the wetland are large (waste

disposal, sand mining, disturbance due to development) and continued pressure may result

in further decline of shorebird assemblages. The results from this study indicate that certain

anthropogenic disturbances, such as waste disposal and sand mining, should be reduced to

maintain and improve the integrity of this wetland.

Keywords Shorebird decline � Community reserve � Habitat loss � India �Anthropogenic pressure � Estuary

Introduction

The world is currently experiencing a rapid decline in species and ecosystems with many

species and populations facing imminent threats of endangerment or extinction (Butchart

et al. 2010; Dawson et al. 2011). The expansion and dominance of humans is likely to

competitively exclude many species (Dawson et al. 2011) with major changes anticipated

in the distribution and abundance of living biota. Anthropogenic climate change is pre-

dicted to exacerbate the situation, with the expansion of ranges of human-tolerant species

and contraction or disappearance of disturbance-intolerant species (Dawson et al. 2011).

Shorebirds can be regarded as global sentinels of such environmental change due to their

migratory ecology and habitat use patterns (Peirsma and Lindstrom 2004). Shorebirds

spend up to two-thirds of the year in migration and on wintering grounds (Burger 1984)

travelling as much as 30,000 km each year (Peirsma and Lindstrom 2004; Recher 1966),

using habitats connecting inland freshwaters and marine environments encompassing

highly variable biomes in widely differing latitudes (Newton 2008). Their life histories

involve taking advantage of seasonally abundant food resources at staging and stopover

areas to build up fat reserves for long distance migration (Recher 1966; Morrison and

Harrington 1979). Furthermore, their use of human-influenced landscapes (such as agri-

cultural land) may help track resilience of species assemblages to direct anthropogenic

disturbance (Peirsma and Lindstrom 2004; Newton 2008; Sundar and Subramanya 2010;

Long and Ralph 2001; Flynn et al. 2009).

Shorebirds are declining worldwide (International Wader Study Group 2003; Huett-

mann and Czech 2006; Stroud et al. 2006) with over 52 % of all assessed species expe-

riencing significant declines (Stroud et al. 2006). Shorebird habitats across the globe have

diminished, with significant portions of the natural habitat lost to agriculture, coastal

development or other anthropogenic modification (Huettmann and Czech 2006). The

Central Asian Flyway (CAF) is shortest of the world’s shorebird flyways, lying entirely in

the Northern Hemisphere. The southern limit of the CAF encompasses the Indian Sub-

continent which serves as wintering areas for many shorebird species (Stroud et al. 2006;

Balachandran 2006). The CAF is also one of the least known flyways, with 80 % of its

shorebird populations being unknown in either size or population trend (Balachandran

2006; Convention on Migratory Species 2005). On different flyways, between 33 and 68 %

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of shorebird populations are in decline, compared with only 0–29 % increasing (Stroud

et al. 2006). The degradation of habitat has also led to the rapid collapse of populations to

below threshold levels (Stroud et al. 2006). In particular, human alteration of habitat has

been coupled with significant increase in pollution, especially in the form of nutrient

enrichment arising from agricultural lands (Balachandran 2006). Most of the wetlands and

rivers in India have high levels of nitrogen, phosphorus, and other nutrients making these

systems extremely eutrophic (see Nagarajan and Thiyagesan 1996; Prasad et al. 2002) and

unsuitable for shorebirds (Kannan and Pandiyan 2012).

Anthropogenic disturbance and nutrient input may influence shorebird distribution and

habitat use patterns. Shorebirds have been found to persist in habitat alongside disturbances

caused by humans (Lafferty 2001). Habitat use by shorebirds is strongly affected by tidal

influence, surrounding vegetation type and amount of standing water (Long and Ralph

2001). Furthermore, agricultural lands are often favored by some shorebird species over

their preferred, natural habitats, making it essential to better understand habitat use patterns

in relation to changes in habitat type (Sundar and Subramanya 2010; Acosta et al. 2010).

Data on habitat loss and shorebird population trends is limited mostly to North America,

Europe, Australia and selected parts of Asia, Africa or South America (Stroud et al. 2006).

The Asian Waterbird Census and other related monitoring works have attempted to reduce

the gap in knowledge of waterbird distributions in Asia (Li and Mundkur 2007); however,

the resolution of this data is limited to bird counts conducted in winter. Analyses of habitat

use patterns by shorebirds and habitat alteration are limited and generally do not incor-

porate long term datasets (Nagarajan and Thiyagesan 1996). Most population estimates are

over 10 years old and current knowledge of shorebird population trends in the CAF is

unknown. The best estimates suggest that a large portion of shorebird populations are

declining in the CAF (Stroud et al. 2006). The threats to shorebirds are poorly understood,

although wetland destruction and depletion of associated food resources are strongly

implied as major factors (Stroud et al. 2006). The main types of habitat destruction are sand

mining, mussel collection, waste disposal and chemical pollution, all of which have been

linked to a reduction in shorebird abundance throughout Asia (Balachandran 2006; Con-

vention on Migratory Species 2005).

To this end, we examined shorebird count data from a wetland in southwestern India

covering an eight-year period to determine changes in the shorebird assemblages in rela-

tion to (i) rainfall patterns; (ii) nutrient enrichment arising from rapid habitat changes

(including waste disposal and sand mining) and (iii) habitat use patterns to better under-

stand the responses of shorebird assemblages in relation to natural and anthropogenic

environmental change.

Methods and materials

Study area

The Kadalundi-Vallikkunnu Community Reserve (KVCR) is one of the four community

reserves in India. The KVCR (11�702800–11�800100N and 75�4903600–75�5002000E, Fig. 1) is

located at the mouth of the River Kadalundi that drains into the Arabian Sea on the west

coast of Kerala. Before entering the sea, the river divides into two channels encircling a

small island. The raised sandbars on the western and southern sides of the island separate

the lagoon from the sea (Uthaman and Namasivayan 1991). Apart from scattered patches

of mangroves, the estuary is bordered by coconut groves and human habitation. Around

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eight hectares of mudflat—exposed during low tides—offer potential foraging ground for

several hundreds of wintering and resident waterbirds, particularly shorebirds. The area

provides significant socio-economic and livelihood services (fishing, oyster farming and

sand mining) for the people living around the estuary. Waterbirds were previously

threatened by hunting in the area (Kurup 1991a, b; Aarif et al. 2011).

Fig. 1 Figure showing the Kadalundi-Vallikunnu Community Reserve (KVCR), Kerala, with distributionof habitat types

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The study area consists of four major habitat types: mudflats, mangroves, shallow water

on mangroves and mudflats and sandy beaches.

Mudflats

Mudflats are fully exposed during low tide. The vertical soil stratum is arranged with mud

at the top 5 cm, then mud with very fine sand and mud with large sand grains at the second

and third 5 cm.

Mangroves

Mangrove forests border the western side of the mudflat. Six species (Avicennia officinalis,

A. marina, Rhizophora mucronata, Kandelia candel, Brugeria cylindrica, Acanthus ili-

cifolius, Exocecaria agalloch) dominate in KVCR (Radhakrishnan et al. 2006).

Shallow water on mudflats and mangroves

Tidal activity creates pools in certain distinct areas of mudflats and mangroves, and these

were defined as shallow water areas.

Sandy beaches

The sandy beaches are located approximately 1.5 km away from the KVCR. A 1.2 km transect

of sandy beach was selected for bird sampling. The adjacent area consists of settlements

occupied by local fishermen. The northern end of the sandy beach contains a boat landing site.

Bird counts

We observed birds from January 2005 to December 2012. Birds were observed at three

scanning points (Mudflats, Mangroves and sandy beaches). The study area was visited once a

week (morning 6–11 am). Observations were made using direct count method and block count

method (Hoves and Bakewell 1989) using binoculars (10 9 50 Nikon) at low tide. Species

were identified using Grimmett et al. (1999), Message and Taylor (2005), Kumar et al. (2005).

Physicochemical variables and rainfall

A water sample (1 L) was taken once a month during low tide from each of the four habitat

types in the study area. Nitrate (NO3-), Phosphate (PO4

2-), Calcium (Ca2?), Potassium

(K?) and Magnesium (Mg?) were quantified using protocols in the American Public

Health Association Manual (APHA 2005). Potassium was quantified by flame emission

photometry while Ca2? and Mg? by complexometric titration. We used Cadmium

reduction technique followed by Spectrophotometer to estimate NO3-, and Molybdate-

Spectrophotometer for PO42-. Rainfall data were collected from a nearby substation

(Centre for Water Resources Development and Management, Kozhikode, Government of

Kerala, India). We assumed that the changes in physicochemical variables were due to

large changes in the human population resulting in waste deposition, chemical pollution

and disturbance, since all of the above variables are typically enhanced in water bodies in

response to anthropogenic pollution (Muzaffar and Ahmed 2007).

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Quantification and statistical analyses

The count data were summarized and categorized by month and year. Count data were

log10-transformed to normalize residuals (Sokal and Rohlf 2012). Monthly measurements

of NO3-, PO4

2-, Ca2?, K?, and Mg? were compared across years to evaluate trends in

chemical composition of the wetland using regression methods (Sokal and Rohlf 2012).

Trends in each of the variables including count data were compared between years using

one-way Analysis of Variance (ANOVA). We used stepwise regression to examine tem-

poral variation in shorebird counts in relation to all environmental variables using the

forward selection procedure with a p \ 0.05 to add variables and p [ 0.10 to remove

variables (Sokal and Rohlf 2012). Total monthly shorebird count was used as the response

variable and annual monthly rainfall, NO3-, PO4

2-, Ca2?, K?, and Mg? as explanatory

variables. Once the most suitable model was determined, the variables for the best model

were retained. We performed one-way ANOVA to determine the relationship between the

previous year’s rainfall and total shorebird counts. Shannon Weiner Index of diversity (H),

species richness, relative abundance (individual species represented as a proportion of the

total number of individuals) and Gini-Simpson’s index were calculated for each year to

evaluate changes in diversity and abundance of shorebirds (Krebs 1989) using PAST

version 2.17 (Hammer et al. 2001). Confidence limits were calculated and pairwise

comparisons between years for each diversity index were carried out using bootstrap

methods with replacement (PAST version 2.17, Hammer et al. 2001). All species that

represented more than 0.5 % of the total number of birds were further analyzed to

determine trends in abundance using linear regression. Total number of shorebirds as well

as relative abundance was calculated for each of the four habitat types (mudflat, mangrove,

sandy beach and shallow). The differences in total counts in each of these habitats were

compared between and within habitats using one-way ANOVAs. Significance (a) for all

statistical tests was set at 0.05. Unless otherwise stated, all tests were performed using

Minitab 14.1 registered to UAE University.

Results

Chemical analyses and rainfall

Regression analysis showed that PO42-, Ca2?, K? and Mg? increased significantly over

the study period whereas NO3- declined (Table 1). The decrease in NO3

- and the increase

in PO42-and Mg? have been gradual, whereas the increase in Ca2? and K? was substantial

and was limited to 2012 (Fig. 2). Only NO3- (one-way ANOVA, F = 8.55, p \ 0.001)

and PO42- (one-way ANOVA, F = 169.49, p \ 0.001) showed a significant declining

trend during the study period. Stepwise regression analysis showed that shorebird numbers

were significantly related to rainfall and NO3- (bird count = 306 ? 213 NO3

-—1.13

rainfall, F = 31.20, p \ 0.001). Additionally, rainfall of the previous year resulted in

significantly lower shorebird counts (one-way ANOVA F = 16.01, p \ 0.001).

Total shorebird count trends and habitat use

Total annual shorebird counts decreased significantly between 2005 and 2012 (one-way

ANOVA, F = 3.63, p = 0.001, Fig. 3a). Mudflats were the most used habitat, with the

percentage of shorebirds counted in mudflats ranging from 37.5 to 67.2 % between 2005

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and 2012. During the same period, the percentage of shorebirds counted in mangroves

ranged from 16.1 to 50.1 %. The declining trends in the percentage of birds using mudflats,

mangroves and shallow water areas showed significant declines (one-way ANOVA,

p \ 0.05 in all cases). In comparison, a significant increase in shorebird numbers was

noted in sandy areas (one-way ANOVA, F = 2.18, p = 0.034, Fig. 3b).

Table 1 Trends in the physicochemical variables over the duration of the study at Kadalundi-VallikunnuCommunity Reserve, Kerala (F and p values from regression analyses are reported)

Trend F p

Nitrate Declining 59.09 \0.001

Phosphate Increasing 11.41 0.001

Potassium Increasing 7.57 0.007

Calcium Increasing 30.58 \0.001

Magnesium Increasing 60.12 \0.001

Fig. 2 Variation in the levels of the five physicochemcical variables (NO3-, PO4

2-, K?, Ca2- and Mg?) inthe Kadalundi-Vallikunnu Community Reserve, Kerala

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Diversity, relative abundance and species trends

Shannon Weiner index values ranged between 0.78 and 1.83 with significant variation

between the years with a generally declining trend (Table 2, Bootstrap, p \ 0.05 in all

pairwise comparisons between years). Richness varied between 17 and 26 species with

significant decline in richness in 2012 compared to all other years (Table 2). Gini-Simp-

son’s index values ranged between 0.47 and 0.52 with significant fluctuations occurring

between years with a declining trend. Six species represented 1 % or more of the total

shorebird population, namely, Lesser Sand Plover (Charadrius mongolus), Greater Sand

Plover (Charadrius leschenaultii), Kentish Plover (Charadrius alexandrinus), Pacific

Golden Plover (Pluvialis fulva), Common Greenshank (Tringa nebularia) and Common

Redshank (Tringa totanus) (Table 3). Lesser Sand Plover was the most dominant species

(67.0–84.6 % of total shorebirds) throughout the duration of the study (Table 3). Of all the

species assessed for trends, eight species (44 %) exhibited significant declining trends

(Table 3). Among the abundant species ([1 % of all shorebirds counted), Lesser Sand

Fig. 3 a Total number ofshorebirds using each of the fourhabitat types in Kadalundi-Vallikunnu Community Reserve,Kerala; and b relative abundanceof shorebirds (%) in differenthabitat types in relation to year

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Plovers, Greater Sand Plovers and Pacific Golden Plovers showed declining trends

(p \ 0.05 in all cases). Additionally, Common Sandpipers (Actitis hypoleucos), Curlew

Sandpipers (Calidris ferruginea), Wood Sandpipers (Tringa glareola), Sanderlings (Cal-

idris alba) and Little Stints (Calidris minuta) showed significant declining trends and were

among the less abundant species (\0.05 % of all shorebirds counted, Table 3).

Discussion

The Kadalundi-Vallikkunnu Community Reserve is an important wintering and stopover

site for birds migrating through the south-western coast of India (Uthaman and Namasi-

vayan 1991; Aarif 2009). The wintering shorebird assemblages in KVCR showed signif-

icant changes in abundance and diversity, which are likely to be linked to natural and

anthropogenic perturbations. Overall, shorebird abundance experienced fluctuations char-

acteristic of migratory waterbirds dependent on water bodies affected by monsoons

(Kannan and Pandiyan 2012; Aarif 2009). Shorebird abundance and diversity declined over

the duration of the study. Abundance was directly linked to rainfall patterns and aquatic

total NO3-. Long-term changes in habitat use patterns were evident in both diversity and

abundance data.

Rainfall and physicochemical variables

The southwest monsoons arising in the Indian Ocean brings substantial rainfall during the

summer months (June–September) across the southern half of India and other parts of

South Asia (Gopal and Chauhan 2001). Additionally, the state Kerala also receives the

north-east monsoon from October to December, although the extent of precipitation may

be limited during this period (Gopal and Chauhan 2001). Expansion of rivers during

monsoon periods causes surrounding river systems to become flooded. Nutrients released

from soil are dispersed over large areas allowing widespread growth of vegetation and

phytoplankton (Gopal and Chauhan 2001; Muzaffar and Ahmed 2007). Resident species of

shorebirds and waterfowl benefit from this abundance of food (Kannan and Pandiyan 2012;

Gopal and Chauhan 2001). Nutrient levels released during the monsoon season decline as

the season progresses (Gopal and Chauhan 2001; Muzaffar and Ahmed 2007). The end of

Table 2 Comparison of the changes in Shannon’s index, Gini-Simpson’s Index and richness in relation toyear (2005–2012) in Kadalundi-Vallikunnu Community Reserve, Kerala

Year Shannon’s index Gini-Simpson’s index Richness

2005 1.20 (1.18–1.21) 0.47 (0.47–0.48) 26 (26–26)

2006 1.27 (1.25–1.29) 0.53 (0.52–0.54) 21 (19–21)

2007 1.14 (1.12–1.15) 0.48 (0.47–0.49) 24 (21–24)

2008 1.04 (1.03–1.06) 0.42 (0.41–0.43) 27 (24–27)

2009 1.09 (1.07–1.11) 0.46 (0.45–0.47) 26 (25–26)

2010 1.08 (1.06–1.09) 0.45 (0.44–0.46) 25 (23–25)

2011 0.79 (0.77–0.80) 0.28 (0.27–0.29) 24 (22–24)

2012 1.15 (1.11–1.18) 0.46 (0.44–0.47) 17 (16–17)

95 % Confidence intervals (derived by bootstrap methods) are shown in parentheses

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the monsoon results in shrinkage of water bodies and lowering of water levels, constraining

nutrient-rich waters into smaller areas (Gopal and Chauhan 2001).The post-monsoon

periods are marked by gradually increasing shorebird numbers, peaking in winter in South

Asia (between December and January) (Kannan and Pandiyan 2012). Extended monsoon

delays the cycle of nutrient release and consolidation of water bodies (Gopal and Chauhan

2001), causing a delay in the arrival of shorebirds in winter as well as an overall reduction

in their numbers (Kannan and Pandiyan 2012). Subsequently, shorebirds begin migration

before the onset of the monsoon (Kannan and Pandiyan 2012; Li and Mundkur 2007)

presumably due to depletion of resources and environmental and biological cues prompting

migration (Recher 1966).

The current study observed high shorebird counts linked to low rainfall in the same year

and in the previous year. This may be due to changes in food resources associated with

alteration to the habitats and increased nutrients in the environment. Shorebirds tend to

migrate in waves, with loosely aggregated assemblages migrating through given areas

(Recher 1966). Total counts may obscure some of the variation in the timing of different

species flying through, to avoid competition for and depletion of food resources (Recher

1966). Additionally, the over abundance of selected nutrients could favor the growth of

certain biota and preclude others (Heip 1995; Muzaffar and Ahmed 2007). For instance,

nutrients released in the early part of the season could cause algal blooms (Muzaffar and

Ahmed 2007), which in turn could influence invertebrate abundance (Gopal and Chauhan

2001; Heip 1995). However, the interaction between nutrient enrichment and benthic

invertebrate abundance is complex and not readily predictable (Heip 1995; Manikannan

et al. 2012). Nutrient enrichment alters benthic invertebrates through an increase in benthic

Table 3 Comparison of population trends in shorebirds in Kadalundi-Vallikunnu Community Reserve,Kerala

Species Scientific name Relativeabundance (%)

Trend F p

Lesser Sand Plover Charadrius mongolus 67.0–84.6 Declining 6.75 0.041

Greater Sand Plover Charadrius leschenaultii 1.5–9.9 Declining 6.22 0.047

Kentish Plover Charadrius alexandrinus 3.4–7.8 Not declining 4.45 0.079

Pacific Golden Plover Pluvialis fulva 0.3–6.8 Declining 6.64 0.042

Common Redshank Tringa totanus 2.0–9.5 Not declining 5.94 0.051

Common Greenshank Tringa nebularia 0.05–5.6 Not declining 0.00 0.961

Whimbrel Numenius phaeopus \1 % Not declining 0.10 0.765

Eurasian Curlew Numenius arquata \1 % Not declining 0.02 0.880

Common Sandpiper Actitis hypoleucos \1 % Declining 35.08 0.001

Dunlin Calidris alpina \1 % Not declining 4.61 0.075

Curlew Sandpiper Calidris ferruginea \1 % Declining 28.46 0.002

Wood Sandpiper Tringa glareola \1 % Declining 7.62 0.033

Terek Sandpiper Xenus cinereus \1 % Not declining 0.34 0.58

Sanderling Calidris alba \1 % Declining 11.9 0.014

Little Stint Calidris minuta \1 % Declining 27.76 0.002

Great Knot Calidris tenuirostris \1 % Not declining 5.28 0.061

Bar-tailed Godwit Limosa lapponica \1 % Not declining 1.73 0.236

Black-tailed Godwit Limosa limosa \1 % Not declining 0.44 0.532

F and p values are from regression analyses for individual species. Bold p values indicate significance

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infaunal biomass (due to an explosion of opportunistic species), followed by a decrease and

disappearance of species (Heip 1995). The nature and extent of such benthic dynamics

remain difficult to quantify and predict (Heip 1995; Gopal and Chauhan 2001; Manikannan

et al. 2012), although a long term decline in benthic or epibenthic species abundance and

diversity may occur in response to enrichment from anthropogenic sources (Heip 1995;

Pardal et al. 2000). High NO3- was correlated with lower shorebird counts, suggesting that

nutrients from surrounding areas could be affecting invertebrate distributions in our study.

One study in the Great Vedaranyam Swamp, a wetland on the east coast of southern India,

showed declines in the abundance of shorebirds associated with many physicochemical

variables (Manikannan et al. 2012). They also suggested that these changes were linked

with changes in benthic faunal abundance. Another study conducted in Panchivaram

mangroves, also along the east coast of southern India documented similar declines in

relation to human activity linked with changes in physicochemical variables (Sandilyan

et al. 2010). Thus, it is likely that changes in the abundance of food resources are linked to

rainfall and selected nutrients.

Changes in diversity and habitat use

The diversity patterns of shorebirds showed an overall declining trend during the study

period. Shannon-Weiner Index and Gini-Simpson’s index values showed significant dif-

ferences in relative abundance of species throughout the period, indicating that the pop-

ulations were highly variable in numbers between years. The sharp decline in diversity

between years 2011 and 2012 was reflected in the richness value only and not in the

Shannon-Weiner or Gini-Simpson’s values. We interpret this as a true decline in species

diversity since both indices used in this analysis may give similar scores based on the

relative proportion of species in spite of a decline in richness. The results from this study

suggest that a threshold level of disturbance and nutrient enrichment was exceeded and

shorebirds responded by decreasing in diversity. Such changes are often influenced by

bottom-up effects, with prey availability being central determinants of predator (shorebird)

abundance (Aarif 2009; Connors et al. 1981; Burger et al. 1997; Drake et al. 2001; Ribeiro

et al. 2004).

Habitat use patterns changed over time in our study. Total shorebird counts indicated a

gradual and significant shift from the use of mostly mudflats and mangroves to the use of

sandy beaches (Fig. 2). As Lesser Sand Plover was the most abundant species throughout

the study, it may be concluded that the species changed habitat use with a shift to the less

preferred sandy beach habitat (Aarif 2009). Habitat use patterns are reflective of ecological

and behavioral differences in species (Aarif 2009; Connors et al. 1981; Burger et al. 1997;

Drake et al. 2001; Ribeiro et al. 2004). The variation in the diversity and abundance could

be linked with ecological variables associated with the prey base. Aarif (2009) showed that

the prey species of Lesser Sand Plovers were different between mudflats, mangroves and

sandy beaches in the same study site. In this study, polychaete worms appeared to be the

preferred prey for Lesser Sand Plovers. Polychaete worms were most abundant in mudflats,

followed by mangroves and were absent from sandy beaches. This abundance was sig-

nificantly related to the mean number of pecks recorded in these same habitats (Aarif

2009). In comparison, crabs were present in all three habitats (mudflats, mangroves and

sandy beaches) and the corresponding number of pecks declined from mudflats, mangroves

to sandy beaches. Many studies document that shorebirds are spatially distributed in

relation to the prey base (Connors et al. 1981; Burger et al. 1997; Drake et al. 2001; Ribeiro

et al. 2004). Shorebird distribution has been correlated against abundance of prey species

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according to habitat type (Ribeiro et al. 2004). Shorebirds that fed on polychaetes (e.g.

White-rumped Sandpipers, Calidris fuscicollis) were abundant in areas with the highest

densities of prey (Ribeiro et al. 2004); similarly, shorebird species that fed primarily of

crabs were most abundant in habitats with high crab densities. Thus, the change in habitat

use of shorebirds (reported for Lesser Sand Plovers) in the present study could be related to

a decline in the overall abundance of polychaetes (Aarif, unpublished data), which could be

associated with nutrient enrichment (e.g., Heip 1995; Pardal et al. 2000).We suggest that

high levels of nutrient input and disturbance has altered the benthic communities of the

intertidal areas in Kadalundi estuary. A reduction in polychaetes creates poorer quality

habitat for shorebird species, forcing them to more productive areas (Burger et al. 1997;

Drake et al. 2001; Ribeiro et al. 2004; Warnock and Takekawa 1995).

The observed change in habitat use could be regarded as resilience (Krebs 1989) of

shorebird assemblages in the Kadalundi estuary. In the face of extreme levels of distur-

bance and anthropogenic nutrient input, the overall shorebird counts have not declined

catastrophically (80.3 %) over the course of the study. Decline in specialist species, such as

Curlew Sandpipers or Dunlins is expected since these species are unable to withstand large

changes in habitat quality and food availability (Huettmann and Czech 2006). Declines in

more abundant, generalist species such as Lesser Sand Plovers, Greater Sand Plovers and

Pacific Golden Plovers suggest drastic changes in the habitat quality and quantity. This

phenomenon is already recorded worldwide for shorebirds and regarded as a significant

long-term problem that needs to be addressed (International Wader Study Group 2003;

Huettmann and Czech 2006, Manikannan et al. 2012). Thus, a steady decline in abundance

and diversity, coupled with changes in habitat use indicates that the system is on the verge

of catastrophic declines and may not be able to host large numbers of shorebirds in the

long-term.

Conservation implications

The Kadalundi-Vallikkunnu Community Reserve is an important stopover area for

migratory shorebirds, and much can be done to protect and support the system. Anthro-

pogenic disturbance, in the form of sand mining, mussel collection and recreational visits

near Kadalundi, are regarded as major threats to foraging shorebirds in the area (Aarif

2009). The larger human population in the surrounding areas have also increased waste

disposal, causing high levels of plastic and other pollution in the estuary. The Kadalundi

River has also been experiencing low flow rates, which may have influenced the nutrient

content of Kadalundi estuary. Additionally, nearby poultry slaughter houses that dump

offals in open dumping areas, have increased the density of raptors (such as Brahminy

Kites, Haliastur indus) and feral predators (such as cats, domestic dogs), which frequently

prey on shorebirds and alter foraging patterns by increasing predator vigilance. Thus a

combination of anthropogenic factors threatens foraging shorebirds in the Kadalundi.

Threats such as these have been widely documented in shorebird habitats and are regarded

as a serious concern in shorebird conservation (International Wader Study Group 2003;

Huettmann and Czech 2006, Sandilyan et al. 2010). Management options must incorporate

plans to reduce and eliminate some of these threats by protecting key shorebird foraging

and roosting areas in Kadalundi. Additionally, illegal activities such as sand mining must

also be prohibited and regulated to reduce detrimental effects on shorebird habitat.

Acknowledgments Authors are thankful to Kerala State Forest Department for Granting research per-mission for our study. Financial support for the study was obtained from Moulana Azad National fellowship

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from University Grant Commission, New Delhi, India. SB acknowledges director Salim Ali Centre forOrnithology and Natural History for the logistic support. We are also thankful to local authorities ofKadalundi for their support in the field.

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