ACTA ORNITHOLOGICA

Vol. 56 (2021) No. 2

Occurrence and behaviour of shorebirds depend on food availability and

distance of beaches from urban settlements

Danilo Freitas RANGEL1, Eduardo Freitas NOBRE DA SILVA2 & Leonardo Lopes COSTA1,*

1Laboratoryof Environmental Sciences, Universidade Estadual do Norte Fluminense Darcy Ribeiro, BRAZIL
2CarlosChagas Filho Institute of Biophysics, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BRAZIL
*Corresponding author, e-mail lopes.bio.mp.sfi@pq.uenf.br

Rangel D. F., Nobre Da Silva E. F., Costa L. L. 2021. Occurrence and behaviour of shorebirds depend on food availability
and distance of beaches from urban settlements. Acta Ornithol. 56: 00–00. DOI

Abstract. Coastal ecosystems provide important feeding opportunities for shorebirds, depending on their prey avail-
ability, hydrodynamic conditions and human pressure. We aimed to evaluate short-term responses (occurrence and
minimum approach distance) of shorebirds to urbanization and natural drivers on an extensive beach arc adjacent to
the largest hypersaline coastal lagoon of South America. The presence of the migrant Sanderling Calidris alba and resi-
dent Collared Plover Charadrius collaris was geo-coordinated and for each record and an equivalent number of random
points we measured the distance from urban settlements, swash width and invertebrate abundance (food availability)
in a snapshot sampling. The distance at which each shorebird flock escaped from humans was determined (minimum
approach distance). The occurrence of shorebirds was predicted by food availability, and higher crustacean density was
found in areas of shorebird occurrence (37 ± 19 individuals/m2) compared to random points (10 ± 10 individuals/m2).
This result highlights the importance of the beach as a feeding area and the need for conservation of shorebirds’ prey.
The resident Collared Plover delayed their escape from humans in areas closer to urban areas, suggesting a higher tol-
erance to humans on disturbed beaches, where they can prioritize the food intake rather than vigilance. The larger
flocks let the researcher get closer, corroborating the risk-dilution theory stating that flocking behaviour during forag-
ing provides protection of birds from predators. In conclusion, our results showed that monitoring of sandy beaches
based on shorebirds’ presence and behaviour can be a reliable tool, especially close to coastal lagoons that constitute
foraging sites for these charismatic species.

Key words: behavioural response, coastal areas, ecological indicators, food availability, snapshot, urbanization

Received — Jan. 2020, accepted — Nov. 2021

INTRODUCTION human disturbances with negative effects for

Resident and migratory shorebirds require coastal
habitats for breeding, nesting, resting and forag-
ing (Brindock & Colwell 2011). Coastal lagoons,
intertidal flats, and other environments with less
harsh hydrodynamics than ocean beaches are
usually the most suitable habitats for shorebird
foraging (Burger et al. 1997). However, ocean
sandy beaches can also provide important feeding
opportunities, depending on the available prey,
usually macroinvertebrates such as polychaetes,
crustacean, mollusks and insects (Schlacher et al.
2016). Urban occupation and habitat loss on sur-
rounding coastal ecosystems have enhanced the
importance of feeding patches on sandy beaches
worldwide (Hubbard & Dugan 2003). Neverthe-
less, sandy beaches are also suffering countless
potential prey (Dugan et al. 2003, Defeo et al.
2009).
Physical and landscape factors regulate the use
of ocean beaches by shorebirds, including hydro-
dynamics (e.g. swash and wave action), sediment
characteristics (e.g. grain size and penetrability),
distance from forest areas and human distur-
bances (Lunardi et al. 2012, Meager et al. 2012).
These environmental characteristics are decisive
for shorebird occurrence on sandy beaches
because of their thermal homeostasis, energy
intake, and predation risk (Dugan et al. 2003,
Yasué 2006, Neuman et al. 2008). Especially for
migrant shorebirds, the energy intake in non-
breeding areas is crucial for the success in the
migration period (Kalejta et al. 1992, Lunardi et al.
2012).
2 D. F. Rangel et al.
Shorebirds perceive humans as potential pred-
ators (Frid & Dill 2002). When humans are pres-
ent, shorebirds deal with constant trade-offs.
Inasmuch as individuals seek to reduce the preda-
tion risk by behavioral responses (e.g. fly away
when there is human proximity), this can result in
temporary stops of feeding, reduced feeding rates
and, consequently, in lower energy intake (Vooren
& Chiaradia 1990, Burger 1994, Yasué 2006). In
addition, depending on the level of human distur-
bance, shorebirds can chronically avoid disturbed
areas (Scherer & Petry 2012) or even habituate to
people (Goss-Custard & Verboven 1993, Yasué
2006). Tolerance to people can be studied by
behavioral measurements such as the minimum
approach distance: the shortest distance in which
a person can get close to wild species before they
escape (Yasué 2006).
Shorebirds have several habitat requirements,
thus their presence or behavior may be early indi-
cators of environmental and anthropogenic influ-
ences in short term assessments (Cuttris et al.
2015, Tavares et al. 2015). Generally, shorebirds
prioritize low-disturbed and food-abundant areas
with environmental characteristics that do not
demand intense vigilance behavior (Thomas et al.
2003). Therefore, the presence of shorebirds on
beaches indicates at least food availability, re-
gardless of the need for long-term monitoring
(Lunardi et al. 2012). Particularly behavioural
responses to human presence are hypothesized to
indicate disturbances in homogeneous ecosys-
tems, where the vigilance behaviour is decisive,
because the interaction between wildlife and
humans is frequent and rapidly perceived by the
birds (Yasué 2006). Sandy beaches constitute,
therefore, interesting study models of responses
of shorebirds to human disturbances. Response of
birds to humans is poorly documented, especially
on subtropical and tropical beaches (Schlacher et
al. 2013). Impact assessments on beaches usually
focus on macroinvertebrates (Costa & Zalmon
2019a) and rarely on their predators (but see
Dugan et al. 2003).
The objective of the present study was to eval-
uate the short-term responses (occurrence and
minimum approach distance) of shorebirds to
anthropogenic and environmental drivers on
sandy beaches. We tested whether shorebird
occurrence and their minimum approach distance
from humans are short-term indicators of envi-
ronmental (food availability and swash climate)
and anthropogenic influences (distance from
urban settlements) on an extensive beach arc in
Southeastern Brazil, which is adjacent to a large
coastal lagoon (shorebird habitat), where intense
human disturbances have caused habitat loss.
MATERIAL AND METHODS
Study area
The Praia Seca Beach Arc, located in Southeastern
Brazil (22°56’S, 42°17’W), was chosen to assess
whether the occurrence and escape behaviour of
shorebirds from humans is related to potential
environmental and anthropogenic predictors.
This beach arc is located in the municipality of
Araruama within an Environmental Protection
Area (Costa do Sol State Park); it is an ecologically
important area for several threatened marine
species (Tavares et al. 2016). The largest (∼220 km2)
hypersaline coastal lagoon in South America
(Araruama Lagoon) is located less than 2 km from
the sampling area on the beach (Fig. 1). The
Araruama Lagoon provides an important staging
and foraging area for migratory and resident
shorebirds (Tavares & Siciliano 2013), however it
has been severely prejudiced by countless human
disturbances, as fishery, chemical pollution, and
urban development (Bertucci et al. 2016, Cruz et
al. 2018).
Sampling
To search for shorebirds on the beach, the inter-
tidal-supralitoral interface was inspected along
~4 km during the morning (between 05:00 and
10:00) and afternoon (between 14:00 and 19:00) in
December 2018 (austral summer) by two
researchers. We selected the summer season for
this snapshot survey (sampling was carried out
within one day) because several migratory shore-
birds leave their breeding grounds in the
Northern Hemisphere to spend the austral sum-
mer in South American. Thus, we were able to
include resident and migrant shorebirds in the
sampling.
Locations of shorebird (single individual or
flocks) occurrence (n = 44) were geo-coordinated
with GPSMAP Garmin (62sc) with at least 5 m
accuracy by walking to the area where the birds
were observed before they flew away. Soon after a
shorebird flock was detected, a minimum
approach distance experiment was conducted to
determine how close a single person could get to
shorebirds before they stopped foraging. The dis-
tance to the flock was estimated (with a measur-
ing tape) from where the researcher stopped,
 Shorebirds’ foraging on ocean sandy beaches 3

70°0’W 60°0’W 50°0’W 40°0’W

10°0’N
0°0’S
10°0’S

Brazil 42°21’0”W 42°19’30”W 42°18’0”W

20°0’S

22°53’30”S
Ararurama Lagoon
30°0’S

22°55’0”S
Rio de Janeiro

43°46’0”W 42°49’0”W 41°52’0”W

22°56’30”S
N
22°46’0”S 21°52’0”S

22°58’0”S

Rio de Janeiro State 1 km Sampling area

Urban settlements

100 km

Fig. 1. Map of the study site showing the Praia Seca Beach Arc located in front of the Araruama Lagoon, in SE Brazil.

immediately before the individuals escaped. The this pool to match the 44 records of birds. After
approximation of the researchers toward the birds collecting data on swash width and invertebrate
occurred parallel to the shore to avoid surprising abundance at each point of shorebird occurrence,
visualization of the researchers by the birds, the closest random point (> 300 m) was immedi-
caused by the presence of berms or any potential ately accessed, and the predictor variables were
inclination on the beach face. The number of indi- measured. Geo-coordinates were utilized in the
viduals in the flocks (flock size) was also deter- measurement of the shortest distance to urban
mined as a potential predictor of the minimum settlements for all points using the Google Earth
approach distance of shorebirds. Bird counting software (accessed 20 December 2018).
events lasted a maximum of five minutes and they To determine the abundance of potential prey,
were carried out in the opposite direction from one sediment sample was taken at each point of
where the birds flew away whenever possible, to shorebird occurrence and at each random point
prevent recounting (Bibby et al. 2000). Bird count- with a PVC corer (20 × 20 cm). The samples were
ing and experiments of minimum approach dis- collected at distances from the waterline similar to
tance were performed at points without beachgo- where the last shorebird occurrence was reported.
ers. The sediment was sieved on a 0.5 mm mesh, the
For each shorebird record (a flock or single organisms were identified at the lowest taxonom-
birds), a random point was selected to measure ic level possible and counted by a single
landscape (shortest distance from urban settle- researcher during 10 min of screening in the field.
ments) and beach features (swash width and The beach macroinvertebrates species are well-
invertebrates abundance), as predictor variables. known in the region (Costa et al. 2017b), making
A bulk of random locations (n = 100) was previ- visual identification in the field possible. The
ously selected using the Google Earth tool. During swash width was determined by the distance of
the field collection, 44 background points in the the sand stretch between the water line and the
intertidal-supralittoral interface were chosen from upper limit of the backshore (Costa et al. 2019).
4 D. F. Rangel et al.

Data analysis Model selection was based on the lowest

Pearson correlation analysis was used to assess the
correlation coefficient (r-value) between predictor
variables. Predictor variable values are expressed
as mean ± standard deviation in the Results sec-
tion. An Analysis of Variance (ANOVA) with 95%
confidence interval was performed to compare
the invertebrate abundance and swash width
between points of shorebird occurrence and ran-
dom points, and according to time of day (morn-
ing vs. afternoon).
Generalized Linear Models (GLMs) with bino-
mial distribution were employed to test the null
hypothesis that the presence of shorebirds on the
beach is random (not related to any predictor vari-
able). The shorebirds presence (1) and absence (0)
were the response variables included in the
GLMs, whilst ‘species’, ‘time’ (afternoon vs. morn-
ing), ‘distance from urban settlements’, ‘inverte-
brate abundance’, and ‘swash width’ were tested
as predictor variables.
Linear Models (LMs) were applied to test the
null hypothesis that the minimum approach dis-
tance of shorebirds (response variable) is not relat-
ed to any predictor variable. The predictor vari-
ables included in the initial LM were ‘species’,
‘time’, ‘distance from urban settlements’, ‘flock
size’ and ‘swash width’. Statistical assumptions of
linear models (normality, linearity and homo-
scedasticity) were confirmed after visual inspec-
tion of residuals.
Akaike information criterion (AIC) values for all
possible combinations of predictor variables
(Table 1). We also included the interaction be-
tween “species” and the most important predictor
variable in GLMs and LMs, to assert if the effect of
such predictor depended on the species. The
analyses were performed using the ‘lme4’ and
‘MuMIn’ packages in R version 3.4.3. (Fox &
Weisberg 2011, Barton 2018).
RESULTS
Environmental characteristics and potential prey
The swash width ranged from 1 to 13 m (9.5 ±
2.0 m). Similar swash width was found in the
areas of shorebird occurrence (9.7 ± 2.1 m) and at
random points (9.4 ± 2.0 m) (F = 0.274, df = 1, 84,
p = 0.60).
The crustaceans Atlantorchestoidea brasiliensis
and Excirolana braziliensis made up the bulk of
macroinvertebrates in the intertidal area (92%).
Polychaetes (1 ± 3 individual/m2) and mollusks
(Donax hanleyanus, 1 ± 2 individual/m2) were less
abundant.
Higher crustacean density was found in areas
of shorebird occurrence (37 ± 19 individuals/m2)
compared to random points (10 ± 10 individu-
als/m2) (F = 58.546, df = 1, 84, p < 0.001). The
same crustacean density (35–37 ± 4 individuals/m2)

Table 1. Summary of model selection results for GLMs or LMs explaining probability of shorebird occurrence (upper panel) or
minimum approach distance (lower panel) on the Praia Seca Beach Arc SE Brazil. For each model: flock — flock size; dist — dis-
tance from urban settelement; swash — swash width; food — prey abundance; spec — species (Calidris alba vs Charadrius collaris);
time — time of day (morning vs afternoon), logLik — model logLikelihood, AIC — Akaike Information Criterion, delta — differ-
ence between the model’s AICc value and the minimum AIC for the whole set of competing models, weight — Akaike weight
for a model. For shorebird occurrence only results for models within delta AIC < 2 are reported, while for minimum approach
distance results for all models analysed are reported.

logLik AIC delta weight

Shorebirds occurrence (Binominal GLM)
food + swash -32.36 70.7 0.00 0.18
food + swash + time -31.46 70.9 0.20 0.17
dist + food + swash + time -31.11 72.2 1.48 0.09
food + swash + spec -32.12 72.2 1.51 0.09
food + time -33.23 72.5 1.73 0.08
food + swash + spec + time -31.35 72.7 1.96 0.07
dist + food + swash -32.36 72.7 1.99 0.07
Minimum approach distance (Linear Model)
flock + dist + swash + spec + time + dist*spec 16.96 -17.9 0.00 0.32
flock + dist + spec + time + dist*spec 15.88 -17.8 0.17 0.30
flock + dist + swash + food + spec + time + dist*spec 17.03 -16.1 1.86 0.13
flock + dist + food + spec + time + dist*spec 15.89 -15.8 2.15 0.11
dist + spec + time + dist*spec 13.47 -14.9 2.98 0.07
dist + swash + spec + time + dist*spec 13.97 -13.9 3.98 0.04
dist + food + spec + time + dist*spec 13.52 -13.0 4.88 0.03
 Shorebirds’ foraging on ocean sandy beaches 5

was found in the areas of occurrence for the two A

shorebird species: the Sanderling Calidris alba and

Probability of finding a shorebird

1.0 0
the Collared Plover Charadrius collaris. Prey abun-
15
dance was also significantly higher in the morn- 0.8 30
ing (42 ± 15 individuals/m2) than in the afternoon

Frequency
(17 ± 14 individuals/m2) (F = 26.707, df = 1, 42, 0.6
p < 0.001). The predictor variables swash width,
0.4
prey abundance, and distance from urban settle-
ments were not correlated (r < |0.4|). 0.2 30
15
Shorebirds occurrence and minimum approach 0.0 0
distance
Two species, the migratory Sanderling (n = 99 0 5 10 15
individuals) and the resident Collared Plover Prey abundance
(n = 246 individuals) were observed during the B
survey. The Sanderling was found in flocks with

Probability of finding a shorebird

1.0 0
an average of six individuals (1 to 15 individuals), 15
and the Collared Plover was found in flocks with 0.8 30
an average of 10 individuals (1 to 34 individuals).

Frequency
0.6
A total of 17 and 24 flocks of the Sanderling and
the Collared Plover, respectively, were reported. 0.4
Single individuals were observed one time for the
30
Sanderling and two times for the Collared Plover. 0.2
15
The prey abundance was the main predictor of
0.0 0
shorebirds occurrence (Table 2). The higher the
food abundance, the higher the probability of
2 4 6 8 10 12
finding a flock or an individual of Sanderling
Swash width (m)
or Collared Plover on the Praia Seca Beach Arc
(Fig. 2A). The probability of finding a shorebird Fig. 2. Probability of finding a shorebird (Calidris alba or Charadrius
also increased under wider swashes (Table 2, collaris) on the Praia Seca Beach Arc, SE Brazil (left vertical axis)
Fig. 2B). Distance from urban settlements, species, as function of prey abundance on the intertidal zone (A) and
and time of day were not significant predictors. swash width (B) according to the Binomial Generalized Linear
Model (black line). The bars represent the invertebrate abun-
The increasing distance from urban settle- dance (right vertical axis) in the shorebirds occurrence points
ments resulted in increasing minimum approach (upper bars) and in random points (lower bars).

Table 2. Parameter estimates for the best models explaining the probability of finding a shorebird (upper panel) and the minimum
approach distance for shorebirds (lower panel) on the Praia Seca Beach Arc, SE Brazil identified in the model selection procedure
(Table 1). Significant predictors of the models are marked in bold.

Estimate SE z p
Shorebird occurrence (Binomial GLM)
(Intercept) -7.049 1.949 -3.617 < 0.001
Food 0.703 0.145 4.837 < 0.001
Swash width 0.428 0.161 2.659 0.008
Null deviance: 119.17 on 85 degrees of freedom
Residual deviance: 64.73 on 83 degrees of freedom
Minimum approach distance (Linear Model)
(Intercept) 23.014 1.811 12.707 < 0.001
Distance from urban settlements (Dist) 0.000 0.000 1.443 0.157
Species (Sps) -0.456 1.299 -3.508 0.001
Flock size -0.077 0.034 -2.260 0.030
Time (morning vs afternoon) -4.595 0.658 -6.986 < 0.001
Swash width -0.192 0.140 -1.372 0.178
Dist × Sps 0.002 0.001 3.805 0.001
Residual standard error: 1.564 on 36 degrees of freedom
Multiple R-squared: 0.7905, Adjusted R-squared: 0.7556
F-statistic: 22.64 on 6 and 36 df, p < 0.001
6 D. F. Rangel et al.

distance of shorebirds (F = 37.608, df = 1, 36, DISCUSSION

p < 0.001). The interaction of this factor with
“species” was also significant (F = 14.369, df = 1,
36, p < 0.001) (Table 2). The individuals of the res-
ident Collared Plover flew away from humans at
shorter distances in areas closer to urban settle-
ments, whilst this pattern was not evident for
Sanderlings (Fig. 3).
Flock size was also a significant predictor
(F = 5.140, df = 1, 36, p = 0.03) of the minimum
approach distance (Table 2). In general, shorebirds
in larger flock sizes tolerated higher human prox-
imity (lower minimum approach distance) than
those in smaller flocks (Fig. 3).
The lowest minimum approach distance val-
ues were found during the afternoon (F = 63.616,
df = 1, 36, p < 0.001) (Table 2), when prey abun-
dance was also lower (Fig. 3). Food availability
was not included together as predictor variables
in the best two models selected by AIC (Table 1).
The presence of the shorebirds and their mini-
mum approach distance from humans in our
snapshot survey were mainly related to food
availability and distance from urban settlements,
respectively. Thus, our hypothesis that the shore-
birds’ presence and their minimum approach dis-
tance from humans are short-term indicators of
the habitat characteristics, was corroborated.
Shorebird occurrence (41 flocks and 249 individu-
als of Sanderling and Collared Plover along 4 km
of beach) in the intertidal suggests that the Praia
Seca Beach Arc is an important feeding site for
migratory and resident shorebirds. The impor-
tance of ocean sandy beaches as feeding sites
for shorebirds on the Brazilian coast has indeed
been stressed by several authors (Vooren &
Chiaradia 1990, Barbieri & Hvenegaard 2008, Petry
et al. 2012).

Afternoon Calidris alba Regression model

Morning Caradrius collaris regardless of species

A B
30

30
Minimum approach distance

Minimum approach distance

25

25
20

20
15

15
10

10

0 1000 2000 3000 4000 0 5 10 15 20 25 30 35

Distance from urban settlements (m) Flock size
C D
30
Minimum approach distance

15
25

Prey abundance
10
20

5
15
10

0 5 10 15 Morning Afternoon
Prey abundance Time of day

Fig. 3. Minimum approach distance of shorebirds (the closest distance in which a person can get close to shorebirds before they
escape, in meters) as function of the distance from urban settlements (A), flock size (B) and prey abundance (C). Sampling was
carried out in morning (l) and afternoon (n). D: Prey abundance in points of shorebirds occurrence according to the time of day.
 Shorebirds’ foraging on ocean sandy beaches
The Praia Seca Beach Arc is located less than
two kilometres from the largest hypersaline
coastal lagoon of South America, Araruama
Lagoon. Araruama Lagoon is recognized as an
essential foraging site for shorebirds in South-
eastern Brazil (Tavares & Siciliano 2013). Never-
theless, Araruama Lagoon has suffered increasing
human disturbances associated with tourism and
urban development that can induce the selection
of adjacent food-rich beaches by shorebirds as an
alternative or main feeding area (Hubbard &
Dugan 2003). The importance of adjacent aquatic
ecosystems such as lagoons, salt ponds, and sandy
beaches under distinct human disturbance levels
need further investigations at landscape scales (as
proposed by Meager et al. 2012). The analysis of
the importance of prey from distinct habitats in
the shorebirds’ diet could be a future direction.
The Praia Seca Beach Arc is also located in a
Marine Protected Area (Costa do Sol State Park),
and receives tourists almost exclusively during the
austral summer (December to March). In addition,
the beaches in the region are directly influenced
by the upwelling phenomena, resulting in high
primary production. Consequently, high abun-
dance of macroinvertebrates is found, especially
in low-disturbed areas (e.g. > 30 crustacean/m2,
Costa et al. 2017a, Suciu et al. 2018). Even though
the beaches along the Praia Seca Beach Arc have
intense wave action, ‘sediment generalist’ crus-
taceans such as Mole Crabs Emerita brasiliensis,
sandhoppers Atlantorchestoidea brasiliensis and
cirolanid isopods Excirolana braziliensis are abun-
dant, providing an optimal feeding opportunity
for fishes and birds (Costa et al. 2017a). Therefore,
to maintain the minimal level of human distur-
bances (mainly seasonal and in small patches) that
currently reach these biodiversity-rich areas, is
pivotal. Recently, all the kiosks were removed
from the backshore as an important management
action aiming to maintain the most natural condi-
tions as possible on the beach.
Our short-term survey was effective in predict-
ing the occurrence of shorebird species on the
Praia Seca Beach Arc. Food availability was the
main positive driver for the occurrence of shore-
birds, regardless of the species and distance from
urban settlements. This result reinforces the
importance of this beach arc as a foraging area for
shorebirds, including the migrant Sanderling, that
has shown declining population sizes since 1972
due to the loss of their primary habitats (Howe
et al. 1989). Brazilian environment authorities
(e.g. Chico Mendes Institute for Biodiversity
7
Conservation — ICMBIO) recognize the impor-
tance of this ocean beach for migratory shore-
birds, but this is the first scientific evidence on its
usage as a foraging site (Barbosa et al. 2019).
Currently, prey abundance has not been depleted
by the human pressure during the summer, but its
disturbance thresholds remain unknown (i.e.
under which specific impact levels and/or types
prey species are not critically threatened).
One of the most outstanding behaviours of
Sanderlings and Plovers is to avoid incoming tides
in the swash zone, moving rapidly up-shore to
reduce inundation risk (Lafferty et al. 2013,
Schlacher et al. 2013). The probability of finding a
Collared Plover or a Sanderling is higher when
the swash is long-lasting and wide, which pro-
vides shorebirds a more secure condition to opti-
mize food intake (Neuman et al. 2008). This
explains the role of swash width as a significant
predictor of shorebird occurrence on the Praia
Seca Beach Arc.
Interestingly, the minimum approach distance
of the shorebirds was significantly related to the
distance from urban settlements, particularly for
the resident Collared Plover. The closer the
distance to urban settlements, the greater the
tolerance of the birds to human approach (lower
minimal distance) was. This differential behaviour
according to the variable human use of the beach
suggests the habituation of the species to people,
a mechanism suggested by other authors (Goss-
Custard & Verboven 1993, Yasué 2006). This habit-
uation is probably more conspicuous in resident
species and in areas where interaction between
birds and local beachgoers is more frequent, such
as on open and homogeneous ecosystems like
beaches (Glover et al. 2011). The question is wheth-
er this apparent habituation of the resident shore-
bird to humans is exerting energetic stress. At a
local scale, if the human disturbance levels were
unsustainable, both resident and migratory shore-
birds would avoid these energetically favorable
habitats (Thomas et al. 2003, Cuttris et al. 2015). For
now, this is not the case in the Praia Seca Beach
Arc, since distance from small urban settlements
did not impair Sanderling and Plover occurrences.
The flock size partially predicted the minimum
approach distance of shorebirds. Larger flocks let
the researcher get closer during our experiments.
This corroborates the risk-dilution theory stating
that an animal in a group reduces its probability of
being singled out by a predator (Foster & Treherne
1981). Theoretically, if a predator has discovered a
group of prey, but can capture only one prey, the
8 D. F. Rangel et al.
chance of a particular individual of being attacked
becomes lower in larger flocks. According to
Beauchamp (2012), birds can also escape more
slowly in denser flocks to avoid collision.
Both of these hypotheses have not been fre-
quently tested with shorebirds and results are
controversial. For instance, Yasué (2005) observed
that greater flock size resulted in lower feeding
rates of the Least Sandpiper Calidris minutilla in
the absence of people. According to the authors
larger flocks may be more likely to disrupt prey
and cause a temporary reduction in mobile prey
availability due to the avoidance response,
impairing birds’ feeding activity. However, the
intertidal zone (where birds were foraging) of the
Praia Seca Beach Arc provides both mobile and
sedentary invertebrates and does not have dense
wrack beds where amphipods and insects can
refuge in. Therefore, prey mobility might not be
the main driver of feeding rate and escape pat-
terns of shorebirds in the region.
Apparently, shorebirds prioritize food intake
rather than vigilance in the afternoon on the Praia
Seca Beach Arc, resulting in lower minimum
approach distances than in the morning. At least
two mechanisms can explain this result. The first
is a possible need to increase food intake follow-
ing an overnight without foraging, specifically for
visual predators such as the resident Collared
Plover (Mcneill et al. 1992). The second is related
to surface activity of potential prey, particularly of
the sandhopper A. brasiliensis, one of the most
abundant macroinvertebrate on the Praia Seca
Beach Arc. Previous studies have shown that the
efficiency of the sediment sampler (our sampling
artefact) depends on the surface activity of mobile
species, being biased during their peak activity
(Costa & Zalmon 2019b). Thus, lower prey abun-
dance in the afternoon might reflect higher sand-
hopper surface activity (and availability for birds).
Surface-active sandhoppers may be easier to be
captured, distracting birds that were foraging by
visual cues and making them less likely to
respond to humans (Yasué 2005).
In conclusion, food availability and distance
from small urban settlements are apparently af-
fecting shorebirds’ occurrence and behavior.
Even with a short-term assessment, it was possible
to use shorebirds’ presence and minimum
approach distance as small-scale ecological indica-
tors of environmental conditions on the beach.
One of the main conservation issues on sandy
beaches is the low potential of endemic fauna,
composed mainly by macroinvertebrates, to raise
awareness for conservation (Harris et al. 2014).
Here, we suggest that shorebirds could be tested
as umbrella and flagship species for conservation
initiatives at regional scales (Maslo et al. 2016).
Shorebirds have several habitat requirements,
among them, prey availability and low levels of
human disturbance. Thus, the protection of shore-
birds’ habitat requirements could result in conser-
vation for co-occurring prey species, becoming
shorebirds’ potential umbrella species (Maslo et al.
2016). In addition, shorebirds are considered
charismatic animals (Maguire et al. 2011), thus
their use as flagship species could support envi-
ronmental education and citizen initiatives aim-
ing to raise awareness for sandy beaches conser-
vation.
ACKNOWLEDGEMENTS
The authors thank the field volunteer Viviane
Gonçalves. LLC is supported by the Coordenação
de Aperfeiçoamento de Pessoal de Nível Superior
— CAPES (88882.463168/2019-01).
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10 D. F. Rangel et al.
STRESZCZENIE
[Występowanie i behawior siewkowych na plaży
zależy od dostępności pokarmu i odległości od
ludzkich siedzib]
Piaszczyste plaże na wybrzeżach morskich mogą
stanowić ważne miejsce żerowania ptaków siew-
kowych, jednak ich wykorzystywanie przez ptaki
zależne jest od dostępności pokarmu, warunków
hydrodynamicznych danego obszaru oraz presji
człowieka. Celem pracy było określenie czyn-
ników wpływających na żerowanie oraz minimal-
ny dystans ucieczki siewek występujących na
rozległej plaży położonej na wybrzeżu Atlantyku,
przyle-gającej do największej hiperhalinowej
laguny Ameryki Południowej — laguny Araruama,
która jest ważnym miejscem żerowania dla
migrujących i osiadłych siewkowych (Fig. 1). Bada-
niami prowadzonymi w grudniu 2018 r. objęto
dwa gatunki — wędrownego piaskowca i osiadłą
sieweczkę płową. Kontrola ok. 4 km odcinka plaży
została przeprowadzona rano (pomiędzy godz.
05:00 i 10:00) oaz po południu (pomiędzy godz.
14:00 i 19:00). Dla każdej obserwacji ptaków (poje-
dynczych lub grup) zapisywano koordynaty
miejsca żerowania ptaków, oraz określano dys-
tans, na jaki mógł zbliżyć się obserwator zanim
ptaki odleciały. Dla każdego miejsca, gdzie zaob-
serwowano siewkowce wyznaczono punkt loso-
wy zlokalizowany powyżej 300 m od miejsca
obserwacji ptaków. Dla miejsc żerowania ptaków
oraz punktów losowych określano: szerokość
strefy zmywania plaży (część plaży cyklicznie
zalewana przez fale), skład gatunkowy i liczeb-
ność bezkręgowców (jako miarę dostępności
pokarmu) oraz odległość od siedzib ludzkich.
Stwierdzono istotnie większe zagęszczenie
skorupiaków (głównie Atlantorchestoidea brasiliensis
z rzędu obunogów oraz Excirolana braziliensis z
rzędu równonogów) w miejscach, w których
obserwowano ptaki (37 ± 19 osobników/m2) niż
punktach losowych (10 ± 10 osobników/m2). Oba
gatunki siewek żerowały w miejscach o podob-
nym zagęszczeniu zdobyczy. Prawdopodobień-
stwo występowania ptaków siewkowych było
związane przede wszystkim z dostępnością po-
karmu oraz szerokością strefy zmywania (Tab. 1, 2,
Fig. 2). Wzrastająca odległość od ludzkich siedzib
zwiększała dystans ucieczki, choć reakcja pta-
ków była specyficzna gatunkowo (Tab. 2, Fig 3).
Sieweczka płowa miała mniejszy dystans ucieczki
bliżej terenów zurbanizowanych (Fig. 3), co może
sugerować wyższą tolerancję na obecność ludzi
na plażach, na których są często przez nich nie-
pokojone. Wynik ten wskazuje, że w takich wa-
runkach priorytetem dla ptaków jest żerowanie, a
nie zachowanie czujności. Na dystans ucieczki
wpływ miały także wielkość grupy ptaków
(mniejszy przy większych stadach) oraz pora dnia
(mniejszy po południu niż rano).
Podsumowując, autorzy wskazują, że dane
dotyczące występowania żerujących siewkowych
oraz ich dystansu ucieczki mogą być wykorzysty-
wane jako wskaźniki warunków środowiskowych
na plażach nadmorskich.