Habitat use by Red Knots (Calidris canutus rufa): Experiments with oyster racks and reefs on the beach and intertidal of Delaware Bay, New Jersey

Accepted Manuscript Habitat use by Red Knots (Calidris canutus rufa): Experiments with oyster racks and reefs on the beach and intertidal of Delaware Bay, New Jersey Joanna Burger, Larry J. Niles PII:

S0272-7714(17)30146-4

DOI:

10.1016/j.ecss.2017.04.025

Reference:

YECSS 5463

To appear in:

Estuarine, Coastal and Shelf Science

Received Date: 6 February 2017 Revised Date:

14 April 2017

Accepted Date: 25 April 2017

Please cite this article as: Burger, J., Niles, L.J., Habitat use by Red Knots (Calidris canutus rufa): Experiments with oyster racks and reefs on the beach and intertidal of Delaware Bay, New Jersey, Estuarine, Coastal and Shelf Science (2017), doi: 10.1016/j.ecss.2017.04.025. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT

Habitat use by Red Knots (Calidris canutus rufa): Experiments with oyster racks and reefs on the beach and intertidal of Delaware Bay, New Jersey

RI PT

Joanna Burgera*, and Larry J. Nilesb

Division of Life Sciences, Rutgers University, 604 Allison Road, Piscataway, NJ, USA

b

Niles and Associates and Conserve Wildlife Foundation of New Jersey, Greenwich, NJ, USA.

*

Corresponding author

M AN U

E-mail address: [email protected] (J. Burger)

SC

a

Rutgers University 604 Allison Road

ABSTRACT

TE D

Piscataway, New Jersey 08854-8082

EP

Sea level rise and increasing human activities have decreased intertidal habitat in many places in the world. The expansion of aquaculture in intertidal areas may impact birds and other

AC C

organisms using these habitats, leading to questions of sustainability of both aquaculture and functioning estuarine ecosystems. Understanding the effect of oyster culture on shorebird activity, particularly on Red Knots (Calidris canutus rufa), a species on the U.S. Threatened List, is important for adaptive management and the expansion of oyster culture. In May 2013 we experimentally compared Red Knot and shorebird use of a beach section with racks and a control, and in 2016 we compared the use of sections with artificial reefs, oyster racks, and

1

ACCEPTED MANUSCRIPT

control on Delaware Bay, New Jersey (USA). The data included only times when no workers or other people were present. Censuses, conducted every 30 min throughout the day (279 censuses in 2013, 231 censuses in 2016), included the number of Red Knots and other shorebirds in each

RI PT

treatment section. In 2013, the total number of shorebirds was significantly higher in the rack section than in the control section, except for Red Knots and Ruddy Turnstones (Arenaria

interpres) that occurred in higher numbers in the control than in the rack section. In 2016 Red

SC

Knot numbers were also significantly lower in the rack section. In 2013, the mean number of Red Knots/census was 13 for racks vs 59 for the control (P < 0.0002). In 2016, the mean number

M AN U

of Red Knots/census was 13 for racks and over 68 for other treatments (P < 0.0001). Treatment, date, and number of non-Knot shorebirds explained 60 % (2013) and 69 % (2016) of the variation in Red Knot numbers. Red Knots avoided the sections with racks while both foraging and roosting, suggesting that caution should be used before placing oyster racks in areas used for

TE D

foraging by Red Knots.

Key words: Artificial reefs, Calidris canutus rufa, Delaware Bay, Intertidal mudflats, Oyster

AC C

EP

racks, Shorebirds

2

ACCEPTED MANUSCRIPT

1. Introduction Climate change and sea level rise affect many aspects of estuarine and coastal habitats, including intertidal mudflats that are used by people and many other species (IPCC, 2007, 2014).

RI PT

There are many competing claims for intertidal space by people, as well as other organisms, and space is decreasing due to sea level rise (Galbraith et al., 2014). Temperate mudflats are used extensively for foraging by nesting and migratory shorebirds, as well as being used by

SC

aquaculture (Kaiser et al., 1998; Solomon and Ahmed, 2016). Many shorebird species spend a quarter of their life migrating between wintering and breeding grounds (Klaassen et al., 2001),

M AN U

making migration stopover areas critical for shorebirds on both northbound and southbound migrations. Since many species migrate from Arctic breeding grounds to wintering grounds in South America, and back, refueling at stopovers is essential (Conklin et al., 2010). During migration shorebirds face habitat loss, prey depletion, severe storms, and disruptions from

TE D

human activities (Butler et al., 2001; Piersma et al., 2001; Burger et al., 2004, 2007; Niles et al., 2008, 2009; Burger and Niles, 2013a, b; Martin et al. 2015). Habitat loss is a function of human development, human disturbance, and sea level rise (Galbraith et al., 2005, 2014; Dill 2017)).

EP

Any factor that reduces either food availability or feeding time jeopardizes reproduction and survival of shorebirds (Baker et al., 2004).

AC C

Most populations of Arctic nesting shorebird species have declined (Morrison et al., 2001, 2007; IWSG 2003; Mizrahi et al., 2012), so understanding the threats facing shorebirds at coastal stopover sites is important. Andres et al. (2012) estimated that 61 % of American shorebird populations have declined in the last 30 years. The declines have been partly attributed to foraging difficulties during migration (Butler et al., 2001; Rose and Nol, 2010), especially at Delaware Bay, New Jersey (Burger et al., 1997; Baker et al., 2013). Human activities can

3

ACCEPTED MANUSCRIPT

decrease foraging success both by pre-empting available habitat, and by disrupting foraging behavior, a distinction often not drawn. Another human activity that could decrease foraging habitat and foraging success is aquaculture, which is increasing in many places in the world,

RI PT

including along U.S. coasts (Kaiser et al., 1998; Solomon and Ahmed, 2016). Decreases in available stopover habitat, decreases in prey availability, and disturbances (raptors, dogs or

foxes, planes and vehicles, aquaculture) contribute to shorebird declines (Harrington et al., 2010;

SC

Burger and Niles, 2013a, b, 2014). Global warming is exacerbating these declines by increasing the risks of migratory flight and altering body size and condition (Van Gils, 2016).

M AN U

In this paper we examine the effect of artificial reefs and oyster racks in the intertidal on foraging shorebirds during spring migration in 2013 and 2016 on Delaware Bay. Despite the widespread use of rack and bag aquaculture, there are few data on effects on shorebirds. Our objectives were to determine: 1) whether treatment (racks, reefs, control) affected the total

TE D

number of foraging shorebirds, or the number of Red Knots (Calidris canutus rufa), and 2) what physical factors explained variation in the number of shorebirds and Red Knots (tide, time of day, date). Examining these factors is important because aquaculture is expanding in many

EP

places in the world, declining shorebird populations may be increasingly dependent upon the same intertidal space required for aquaculture, and Red Knots are federally “Threatened” in the

AC C

U.S. A previous study in Delaware Bay indicated that the presence of racks, activities of workers, and tidal cycle influenced the number of Red Knots, making it difficult to separate the effects of people from the racks alone (Burger et al., 2015). The 2013 data were reanalyzed using only the censuses that included no human activity. In 2016 the racks were not tended, and the experimental area was generally free from human activities. In both years the beach was closed to the public by the state of New Jersey. We were interested in foraging Red Knots

4

ACCEPTED MANUSCRIPT

because of their population declines and their recent federal listing (Dey et al., 2011, 2014; FR, 2014; USFWS, 2016).

RI PT

2. Background

In many parts of the world, shorebirds feed on mudflats at falling and low tides, and are forced to other places or to roost at high tide because of lack of foraging space (Burger et al.,

SC

1977; Pitelka, 1979; Connors et al., 1981; Warnock et al., 2002; Burger and Niles, 2014). The situation at Delaware Bay is different. Northbound shorebirds stop at Delaware Bay only for the

M AN U

month of May to refuel for further northward migration, and they forage almost exclusively on Horseshoe Crab eggs. At high tide Horseshoe Crab eggs are abundant and easily obtained at the tide line (Tsipoura and Burger, 1999). However, feeding must go on throughout the tidal cycle for the birds to gain enough weight for successful migration to the Arctic (Baker et al., 2004). At

TE D

low tide, eggs are scattered over the sandflats with the receding tide in wavy green rows. Most studies over the last two decades on Delaware Bay were of shorebird foraging behavior during high tide when spawning Horseshoe Crabs are concentrated at the tide line. However, the

EP

importance of Red Knot foraging on exposed, intertidal mudflats may have been underestimated. Understanding the effects of all human activities, including aquaculture on the intertidal

AC C

mudflats, can contribute to conservation and the maintenance of stable shorebird populations (Dolman and Sutherland, 1995; Piersma et al., 2006), particularly given decreases in available exposed mudflat due to global climate change (Galbraith et al., 2014). Adaptive management of foraging shorebirds requires the evaluation of methods and strategies to reduce effects of all human activities. In this case, the effects of the structures of rack and bag aquaculture need to be clearly identified before there is expansion into shorebird foraging habitat

5

ACCEPTED MANUSCRIPT

Foraging shorebirds could avoid oyster rack structures and/or they could be disturbed by the presence and activities of the oyster culture workers (Kaiser et al., 1998; Solomon and Ahmed, 2016). An indirect effect of such structures and activities could be a change in prey abundance

RI PT

or diversity (Spencer et al., 1996, 1997; Ferriss et al., 2016). Aquaculture can cause organic enrichment, reduced macrofaunal diversity, and increased biomass (Castel et al., 1989; Nugues et al., 1996). In Humboldt Bay (California), some species of shorebirds were more abundant near

SC

oyster culture racks, while others were not (Connolly and Colwell, 2005). Kelly et al. (1996) reported that Dunlin (Calidris alpina) and ‘peeps’ avoided the rack and bag oyster culture in

M AN U

Tomales Bay. California. Different shorebirds as individuals or flocks respond differently to oyster culture. Studies on the effects of oyster culture structures on birds in an Irish estuary found few differences in distribution, except for the foraging locations of birds around structures (Hilgerloh et al., 2001). However, Hilgerloh et al. (2001) observations were made on only 4

TE D

days, and the number of birds present was relatively small (fewer than 100 birds of any species, medians less than 20, no Red Knots). Dumbauld et al., (2009) found that structures changed the habitat at a landscape scale, which could affect both the prey base and the efficiency of foraging

EP

shorebirds. Changes in sediment are important because Philippe et al. (2016) demonstrated that sediment structure strongly explained the abundance and biomass of Red Knot prey in an

AC C

intertidal mudflat in France.

The traditional oyster harvesting from natural sub-tidal oyster reefs is an important part of Delaware Bay culture (Niles et al., 2013), and finding methods of fostering oyster culture while reducing effects on foraging shorebirds is an important societal goal. The rack and bag method of oyster culture, started in the 1990s, has the potential to aid restoration of Delaware Bay beaches and ecosystems (Gittings and O’Donoghue, 2014; Munroe and Calvo, 2015), but it also

6

ACCEPTED MANUSCRIPT

has the potential to increase erosion and decrease intertidal foraging space for shorebirds, as well as subtidal foraging and resting places for Horseshoe Crabs (Burger et al., 2015). Aquaculture has the potential to meet the growing need for seafood around the world, and to improve local

RI PT

economies (Subasinghe, 2006). However, proposed increases in oyster culture on the intertidal of Delaware Bay also may pose a threat to foraging shorebirds (Burger et al., 2015), suggesting a need to examine the effect of rack and bag oyster culture. Our previous work found that Red

SC

Knots were more sensitive to the presence of people along beaches than were other species

(Burger and Niles, 2013a), as well as being more sensitive to oyster culture activities (Burger et

M AN U

al., 2015).

3. Methods 3.1. Overall design

TE D

Our overall design was to compare Red Knot and other shorebird use of beach sections having oyster racks with controls having no racks. In 2013, there were two treatments: oyster racks and control, and in 2016 there were four treatments: 2 reefs, 1 reef, racks, and control (Fig.

EP

2). The data analyzed from the 2013 experiment included the same geographical area as used in 2016, and excluded any censuses with oyster workers (Burger et al., 2015). A second control

AC C

site used in 2013, south of Reeds Beach South, was not included in the re-analysis because it was on the other side of a wide creek and conditions differed. Our goal in comparing 2013 and 2016 was to examine the effect of racks (no tending) on the number of foraging Red Knots and other shorebirds and to determine if Red Knot response was similar between years.

3.2. Site description

7

ACCEPTED MANUSCRIPT

Delaware Bay is bounded by New Jersey and Delaware (Fig. 1), and is fed by the Delaware River. The Bay is a huge petrochemical port complex, including Wilmington and Philadelphia, and the densely populated upper Bay contributes storm-water overflow. Several

RI PT

rivers enter the bay, and some of the smaller creeks provide important mudflats for foraging shorebirds during low tide. Delaware Bay is one of the premier stopover sites for Red Knots and other shorebirds on their northward, spring migration (Niles et al. 2008, 2009; Burger and

SC

Gochfeld, 2016). Each year tens of thousands of shorebirds gather at the tideline to forage on eggs of Horseshoe Crabs (Botton et al., 1994, 2003). Along the New Jersey side of Delaware

M AN U

Bay, the intertidal mudflat can be up to 300-400 m wide at low tide.

3.3. Experimental design

In 2013 there was an experimental rack and bag oyster array deployed by a local fisherman,

TE D

and he placed oysters on these racks at Reeds Beach South. Treatments were 1) oyster rack section, and 2) control (adjacent to the oyster rack section). No fences were used to demark the

EP

two sections. The oystermen returned periodically to check the racks and tend the oysters (Burger et al. 2015).

AC C

In 2016 we divided the same beach into four sections 27-30 m wide (89-100 ft) that had different treatments (Fig. 2 and 3). For the experiment we built oyster racks and artificial oyster reefs in the intertidal at Reeds Beach South, and observed the presence of Red Knots and other shorebirds in these experimental treatments and in an adjacent control. The racks and bags simulated the racks used for commercial oyster culture along Delaware Bay. The artificial reefs (parallel to the shore) were used to test whether reefs prevent shorebirds from foraging, prevent Horseshoe Crabs from spawning, and dampen waves that might disrupt spawning or foraging 8

ACCEPTED MANUSCRIPT

shorebirds on the beach. The reefs were built a year earlier than the oyster racks due to permitting issues, but all were in place before 1 May 2016. We had predicted that the reefs would prevent the erosion of sand from the spawning beaches by dampening the amplitude and

RI PT

force of storm waves (as happened during Hurricane Sandy, Niles et al., 2013). Horseshoe Crabs do not spawn when there is a strong surf and large waves because they can be overturned on the beach, and become vulnerable to predation by gulls or desiccation by the sun.

SC

Treatments for the sections in 2016 were 1) two parallel artificial reefs, 2) one artificial reef, 3) racks with bags and shells, and 4) a control (Fig. 2 and 3). Fencing demarcating sections

M AN U

extended from high tide to the outermost edge of the treatments into the intertidal to prevent Horseshoe Crabs from moving among treatments. Stakes securing fencing were about 3 m apart, allowing us to determine the distance of birds from high tide. Reeds Beach South has an

3.4. Protocol and analysis

TE D

intertidal extent of only about 110 meters at the lowest low tides.

Our protocol was to census the number of shorebirds in each treatment at all times of day and

EP

for all tide stages from early May, when shorebirds arrived, until the end of May. In the 2016 analysis we truncated the data after 24 May because Red Knots moved to congregate along the

AC C

creek shoals prior to leaving for the Arctic (departure began 25 May). Thus no data after 25 May 2016 were included in the analysis. We recorded the number of each species of shorebirds that were present on each section of the beach under the different treatments. We also recorded the numbers of Laughing Gulls (Leucophaeus atricilla, formerly in the genus Larus) and other gulls present. We usually conducted a census every 30 min; a census involved counting the number of

9

ACCEPTED MANUSCRIPT

Red Knots and other shorebirds in each treatment section. In 2016 we recorded the number of roosting shorebirds separately. The analyses are based on 279 censuses in 2013 and 231 censuses in 2016, usually from 600

RI PT

or 630 AM to 6 to 8 PM. For example, in 2016 we counted shorebirds in each of the four

sections 231 times. In both years censuses were conducted nearly every day, at all times of the day. We recorded data for Red Knot, Ruddy Turnstone, Semipalmated Sandpiper (Calidris

SC

pusilla), Sanderling (Calidris alba) and Dunlin. We assigned a tide height variable to each observation using tide charts. Any census taken from the time of low tide to 1 hr after was

M AN U

assigned a tide time of 1 hr; from 1 to 2 hours after low tide was assigned a tide time of 2, and so on.

We provide several measures of use: 1) percent of all censuses when shorebirds were present, 2) overall mean number shorebirds present by treatment (for all censuses, including zeros), 3)

TE D

percent of all censuses when Red Knots were present, and 4) overall mean number of Red Knots only for censuses with shorebirds present (Red Knots were only present when other shorebirds were present). We also provide the maximum number of shorebirds (and Red Knots) present on

EP

any one census.

Data were analyzed using non-parametric analysis of variance Kruskal Wallis X2 test, PROC

AC C

NWAY, SAS, 2005). We used these non-parametric tests because they are more conservative and are best suited for small datasets (Siegel, 1956). We also developed models to examine the factors affecting the number of birds present (PROC GLM, SAS, 2005) for both the 2013 and the 2016 data (using only censuses where no people were present). The following variables were used: treatment, time of day, hours before or after high tide (1-6), tide direction (+ or -), date, interactions, the number of gulls, and the number of Laughing Gulls. The models for total

10

ACCEPTED MANUSCRIPT

shorebirds were run using all census periods (including zeros). Since Red Knots were not present in the experimental area unless other shorebirds were present, the models for Red Knot only used censuses where other shorebirds were present. Laughing Gulls were included because

RI PT

some people believe that competition with Laughing Gulls is decreasing foraging opportunities for Red Knots.

SC

4. Results

4.1. Factors affecting presence of total shorebirds and Red Knots

M AN U

Generally the number of shorebirds on Delaware Bay is low in early May, increases to midMay, and declines sharply after about the 25th of May as shorebirds leave for the Arctic. Superimposed on the rise (early May), and decline (late May) in number of shorebirds and Red Knots, was daily variability since shorebird flocks move among beaches. The pattern of use by

TE D

shorebirds and Red Knots in our experimental study area was similar for 2013 and 2016 (Figs. 4). The pattern of use of the oyster rack area was similar to that of the other treatments, but there were many fewer total shorebirds and knots using the rack section. That is, the number of knots

EP

was correlated with the number of shorebirds present. Generally there were fewer shorebirds present in our experiment in 2013 compared to 2016. 2016 was unusual because almost no

AC C

Horseshoe Crabs spawned from 12-15 May because of heavy surf. Thus, there were fewer shorebirds from 10-15 May, more thereafter, and almost none after 24 May 2016. Tide was an important variable, but is not graphed because tide is known as a significant variable. Generally there are more shorebirds present on the Delaware beaches at high tide because they feed on the concentration of eggs due to the mass of spawning Horseshoe Crabs.

11

ACCEPTED MANUSCRIPT

Treatment (racks, reefs, control) was the variable the experiment was designed to examine, and it entered significantly for the total number of shorebirds present (2016), and the total number of knots present (both years). The percent of censuses with shorebirds present did not

RI PT

vary greatly among treatments; it varied from 68.7 % for oyster racks to 78.4 % for the two artificial reef sections (Table 1). However, the mean number of total shorebirds, the mean

number that were foraging, and the mean number that were roosting varied significantly by

SC

treatment (Table 1). There were significantly fewer in the rack section than in the other three treatments. The maximum numbers present also varied markedly (with lower maximum counts

M AN U

in the rack section).

The percent of censuses with shorebirds that also had Red Knots did not vary markedly among treatments (except for roosting Red Knots, Table 2). However, the mean number of Red Knots varied significantly by treatment for all knots, for foraging knots, and for roosting knots.

TE D

There were fewer knots in the section with racks compared to the other sections (Figs. 3 and 4). The maximum numbers present also varied markedly as a function of treatment (Table 2). The

EP

lowest maximum flock size was in the rack section.

4.2. Models explaining variation in numbers

AC C

In 2013, the best models explained 47 % of the variation in the total number of shorebirds as a function of date, the interaction of treatment X date, and the number of Laughing Gulls, while the best model for Red Knots explained 60 % of the variation as a function of treatment, the interaction of treatment X date, and the number of non-knot shorebirds (Table 3). There were significantly more total shorebirds in the oyster rack section (Table 1), but there were significantly more Red Knots in the control section than in the oyster rack section (Table 2).

12

ACCEPTED MANUSCRIPT

In 2016, the best models explained 40 % of the variation in the total number of shorebirds as a function of treatment, tide time, date, time of day, and treatment X date, but not the number of gulls (Table 3). The best model for the number of Red Knots explained 69 % of the variability in

RI PT

terms of treatment, date, and number of non-knot shorebirds (Table 3). Tide did not enter

because the total number of other shorebirds entered (and tide was a highly correlated with the total number of shorebirds present). However, if the number of non-knot shorebirds is not

SC

included in the model, only 25 % of the variance is explained by date in May, time, tide and treatment.

M AN U

The total number of non-knot shorebirds present was a significant factor explaining variation in the number of Red Knots in the study area in both years (Table 3). Knots were generally not present when there were no other shorebirds present. The correlation (2016) between the number of knots and other species varied, and was highest for Ruddy Turnstone (r = 0.61),

TE D

followed by Semipalmated Sandpiper (r= 0.47), Sanderling(r=0.26) and Laughing Gulls (r=0.07), all significant at the P < 0.0001. Partly this reflects positive associations, and partly a common attraction to the presence of Horseshoe Crab eggs. Correlations were not computed for

EP

2013 because knots were present during far fewer censuses. The association with Laughing

AC C

Gulls was positive; there were more Laughing Gulls when there were more shorebirds.

5. Discussion

The data presented in this paper clearly indicate that Red Knots did not use the rack section as much as the other sections. While the knots avoided the rack section, they did use the sections with artificial reefs. We had expected that Red Knot and shorebird numbers would be highest in the control section, and might have been similar in the rack and reef sections because

13

ACCEPTED MANUSCRIPT

both are structures in the intertidal. However, this was not the case in 2016. At low tide, Red Knots and shorebirds fed close to the reefs, and stood on the reefs, but did not stand on the racks or feed near them (Fig. 3).

RI PT

In the intertidal zone, shorebirds could be disturbed by workers, the structures, or a

combination of both (Kaiser et al., 1998; Solomon and Ahmed, 2016). Direct effects could

include avoidance of structures and/or of workers, or the entire area where oyster culture occurs.

SC

An indirect effect of oyster culture could be a decrease in foraging time, rate or efficiency, or a change in prey abundance or diversity (Spencer et al., 1996; Ferriss et al., 2016). Oyster culture

5.1. Possible causes of treatment effects

M AN U

could either decrease or increase prey abundance or diversity, which bears testing.

There are several possible explanations for lowered use of the rack section: 1) Red Knots

TE D

and other shorebirds avoided the rack treatment because it was an inner treatment, 2) Red Knots preferred foraging on the northern part of the beach (the northernmost sections were the 2-reef and 1-reef sections), 3) Red Knots did not prefer the southern sections of the study area, 4)

EP

Horseshoe Crabs may avoid the rack section, or be prevented from spawning on the beach, thus there would be fewer eggs there, 5) timing of construction of the racks and reef, and overall

AC C

experimental design, 6) appearance of the racks was disturbing, and 7) Red Knots avoided the racks as a result of past learning or experience associated racks with disturbance. These were not tested directly, and provide direction for future research. Each will be discussed briefly below. One might argue that shorebirds, and Red Knots, use the end sections more easily than the inner sections, but there was no significant difference between the three other treatments, one of which was also in the middle.

When shorebirds and Red Knots come to forage on Reed’s

14

ACCEPTED MANUSCRIPT

Beach south, they either fly from the south along the shore, or they fly from the north; they do not fly overland. Although there is some movement across Delaware Bay, we never observed this at our study sites in either year. If there was a flight directional effect, then both internal

RI PT

sections in 2016 should have had equally low numbers, and this was not the case.

Another possible explanation was that Horseshoe Crabs might be less likely to spawn on beaches with the racks, which would result in fewer available eggs for shorebirds. However, we

SC

observed Horseshoe Crabs moving under the racks and around the racks, and there were no

differences in the number of Horseshoe Crab egg masses in the upper intertidal or in the samples

M AN U

a few cm below the surface (J. Smith, Unpubl. data). Therefore, the differences in shorebird (and Red Knot) numbers do not appear to be due to differences in prey availability, but this requires further study.

The reefs were constructed over a year earlier than the oyster racks due to a delay in approval

TE D

for construction of the racks. The reefs therefore had a longer period for establishment of an invertebrate community on them, which could provide food for shorebirds. A preliminary study of invertebrates in the sections in 2016 did not show a significant difference (Ivana Novcic,

EP

Unpubl. data) Further there were 4 sections in the 2016 experiment: control, racks, one-reef, and two-reefs. Because of permitting issues, the control and 2 reef sections were 30 m (100 feet)

AC C

across, and the other two sections were 27 m (89 feet) across. The slight difference in length was not evident to human observers in the field, however it could have affected shorebird use of these areas. We believe it did not affect use because there was no significant difference between the 1reef, 2-reef and control sections (which differed in size). It could also be argued that to reach the rack section, shorebirds had to cross 2 fences when flying north, or 3 fences when flying south

15

ACCEPTED MANUSCRIPT

from Reeds Beach North. However, the number of fences shorebirds had to cross to reach the 1reef treatment was the same as the rack section. The appearance of the racks themselves may be disturbing for some reason we have not yet

RI PT

identified; perhaps the vertical structure of the racks reduces predator detection. This appears not to be the case as Red Knots did feed in the rack section when the racks were exposed. There

racks themselves (although they did feed near the reefs).

SC

were just far fewer, they did so much less often, and they did so only at the tide line, not near the

There may be other explanations we have not discussed above, but we believe that it may be

M AN U

a combination of previous experience and learning. Red Knots can live for19 years or more (Baker et al., 2013), and birds clearly learn to avoid certain human activities (Burger and Niles, 2013a,b.; Martín et al., 2015) There is an extensive literature on shorebirds, including Red Knots, which demonstrates that birds are adversely affected by the presence of people, activities,

TE D

and structures. Red Knots prefer places to forage and roost where there are few or no people, and little or no activities (Burger et al., 2004, 2015; Burger and Niles, 2013a). Red Knots may be more sensitive than other shorebirds to the activities around oyster racks. For example, there

EP

were more other shorebirds around racks than the control in 2013, but not in 2016 (there were fewer Red Knots in the rack section in both years).

AC C

While there were no oyster worker activities in our experiment in 2016, only a few km south there is a flourishing oyster culture industry, where oyster workers, equipment, tractors, and power washers are active many days a week during low tide. It is likely that Red Knots have had experience with foraging around or near these oyster racks, or with the disturbances caused by workers tending these racks. Some of these operations occur over many hours, with many people, with several vehicles, and with high-powered (and noisy) washing equipment. Red Knots

16

ACCEPTED MANUSCRIPT

arriving to feed on a section of beach with operating racks have a likelihood of being disturbed. It would seem unusual that Red Knots would not remember this association. They remember how to fly thousands of km to wintering and breeding grounds, and thousands of km to reach

RI PT

Delaware Bay (Niles et al. 2008, 2010). We postulate that: 1) shorebirds suffering frequent disturbance while feeding on beaches or intertidal mudflats with oyster culture activity, associate the racks with disturbance, and 2) when Red Knots move to Reeds Beach for feeding they

SC

maintained the visual association and avoided the rack section where disturbance might occur. In some cases birds habituate to human activity/structures (Nisbet, 2000; Madsen and

M AN U

Boertmann, 2008). Frequent human disturbance, however, leads to abandonment (Smit and Visser, 1993), including a threshold where birds are always disturbed (Goss-Custard et al., 2006). There is no reason to assume that Red Knots and other shorebirds would not learn that “racks” mean frequent human disturbance, and are thus not attractive, whether or not they have

TE D

human activity. One additional point bears mentioning. There were significantly fewer Red Knots in the rack section even at high tide when the racks were covered, which further supports learning their landscape environment.

EP

Finally, the few studies examining the effect of aquaculture on shorebirds have found species-specific differences – some species are more sensitive than others. Clearly, determining

AC C

the effect of rack and bag agriculture on Red Knots must involve study of Red Knots themselves, and their responses in relation to other shorebirds. The Precautionary Principledemands that no new racks be placed in prime shorebird foraging areas without further study to ensure that shorebirds, and particularly the threatened Red Knot, is not adversely affected (Burger, 2003).

5.2. Overall shorebird numbers and the presence of zeros

17

ACCEPTED MANUSCRIPT

The mean number of Red Knots present, particularly in 2016, was quite high. That is, Red Knots were present on from 34 % to 53 % of the censuses, mean numbers averaged up to 80 per section, and maximums were as high as 1315 Red Knot per section. Numbers were lower in

RI PT

2013. We suggest that the relatively high numbers in 2016 were due to a concentration of

spawning Horseshoe Crabs on Reeds Beach South (a restored beach, Niles et al., 2013), and to wind and wave conditions that made foraging there easier (this beach area was more protected).

SC

It should also be noted that the high counts for the different sections in 2016 did not occur on the same day.

M AN U

Since shorebird flocks are highly mobile, shorebird censuses traditionally have a relatively high percentage of zeros. Thus we expected that many of the censuses would be zero, leading to high variance in mean numbers. However, in all treatments combined in 2016, some shorebirds (usually Semipalmated Sandpipers) were present from 69 to 78 % of the time. For the total

TE D

number of censuses, however, Red Knots were present only 13 % to 17 % of the censuses in 2013, and 34 % to 53 % of the censuses in 2016.

EP

5.3. Possible fitness consequences

Examining the effect of human activities on shorebirds usually involves observing the

AC C

immediate effects of people on behavior of individual shorebirds (Stillman et al., 2007; Tarr et al. 2010). Shorebirds decrease foraging or fly away from some activities (Burger et al., 2004; Yasue, 2005; Burger and Niles, 2013a,b, 2014), resulting in decreased foraging time. Decreases in foraging time can have long-term effects on individual fitness. Gill et al. (2001) suggested that behavioral responses alone may not reflect population consequences. However, disruptions to oystercatchers (Haemoatopus ostralegus), mainly from raptors, interfered with foraging time

18

ACCEPTED MANUSCRIPT

and significantly reduced their fitness (Goss-Custard et al., 2006; Goss-Custard, 2014). This suggests that any substantial disturbance that decreases foraging (time, efficiency) could have fitness effects (Dolman and Sutherland, 1995; Morrison and Hobson, 2004). Landscape-scale

RI PT

losses of foraging areas due to mechanical harvesting of cockles (Cerastoderma edule) led to decreases in weight gain, survival, and population levels of Red Knots in the Wadden Sea,

Netherlands (Kraan et al., 2009). These studies should be repeated for other shorebird species,

SC

but a precautionary approach may be needed that involves establishing a baseline of relevant scientific studies that provide information to public policy makers, managers, and the public

M AN U

before making radical ecologic changes in the ecosystem (Burger, 2003; Dumbauld et al., 2009).

Acknowledgments

We thank Amanda Dey and others at Delaware Bay for monitoring shorebirds and

TE D

providing data on shorebird use at low tide, Joe Smith, Stephanie Feigin, Mark Field, Michael Gochfeld, and Emily Hofmann for field assistance, Taryn Pittfield and Christian Jeitner for technical analysis, and Humphrey Sitters and Nellie Tsipoura for comments on the ms. This

EP

study was funded by the American Littoral Society, Rutgers University, Conserve Wildlife of New Jersey, and Tiko Fund. None of the funders had input into content of the manuscript, and it

AC C

did not require their approval.

19

ACCEPTED MANUSCRIPT

Figure Legends

USA.

RI PT

Fig. 1. Map showing the location of Reed’s Beach study area on Delaware Bay, New Jersey,

photograph showing the experimental design in 2016.

SC

Fig. 2. Diagram of the design for sections with oyster racks, 1-reef, 2-reefs, and a control; and a

M AN U

Fig. 3. Photographs of the experiment in 2016 at Reed’s Beach South, New Jersey, showing the overall design (4a); shown are the sections with one reef, racks, and the control (most distant). Shown also is the reef sections at low tide, with Red Knots and Turnstones standing on the reef and in the shallow water of the intertidal (4b), one of the reef sections with knot and turnstones

TE D

on and near the reef (4c), and the experiment at high tide when no Red Knots were present and rough waters prevented Horseshoe Crabs from spawning.

EP

Fig. 4. Mean number of shorebirds as a function of day (top) and Red Knots as a function of day (bottom) for the main shorebird migration period at Reeds Beach, Delaware Bay, May 2016.

AC C

The low numbers May 13-15 reflects high winds, rough waves, and no Horseshoe Crab spawning.

20

ACCEPTED MANUSCRIPT

References Andres, B.A., Smith, P.A., Morrison, R.G., Gratto-Trevor, C.L., Brown, S.C., Friis, C.A., 2012.

RI PT

Population estimates of North American shorebirds. Wader Study Group Bulletin, 119, 178–194.

Baker, A.J., Gonzalez, P.M., Piersma, T., Niles, L.J., deLima, I., Nascimento, D.O., Atkinson, P.W., Clark, N.A., Minton, C.D.T., Peck, M.K., Aarts, G., 2004. Rapid population decline in red

SC

knots: fitness consequences of refuelling rates and late arrival in Delaware Bay. Proceedings of

M AN U

the Royal Society of London, 21, 875-882.

Baker, A., Gonzalez, P., Morrison, R.I.G., Harrington, B.A., 2013. Red Knot (Calidris canutus). In A. Poole [Ed], The Birds of North America. Online Cornell Lab of Ornithology, Ithaca, NY. http://bna.birds.cornell.edu.bnaproxy.birds.cornell.edu/bna/species/563 (accessed January 3,

TE D

2017).

Botton, M.L., Loveland R.E., Jacobsen, T. R., 1994. Site selection by migratory shorebirds in

EP

Delaware Bay, and its relationship to beach characteristics and abundance of Horseshoe Crab

AC C

(Limulus polyphemus) eggs. Auk, 111, 605–616.

Botton, M.L., Shuster Jr. C.N., Keinath J.A., 2003. Horseshoe Crabs in a food web: Who eats whom? In: Shuster Jr, C.M., Barlow, R.B., Brockman, H.J., (Eds.), The American Horseshoe Crab. Harvard University Press, MA, pp. 133-153.

21

ACCEPTED MANUSCRIPT

Burger, J., 2003. Making decisions in the 21st century: Scientific data, weight of evidence, and the Precautionary Principle. Journal of the International Union of Pure and Applied Chemistry.

RI PT

Implications of Endocrine Active Substances for Humans and Wildlife, 75, 2505-2513.

Burger, J., Gochfeld, M., 2016. Habitat, population dynamics, and metal levels in colonial

SC

waterbirds: a food chain approach. CRC Press, NY, USA. 565 pp.

Burger, J., Niles, L., 2013a. Shorebirds and stakeholders: effects of beach closure and human

M AN U

activities on shorebirds at a New Jersey coastal beach. Urban Ecosystems, 16, 657-673.

Burger, J., Niles, L., 2013b. Closure versus voluntary avoidance as a method of protecting

TE D

migrating shorebirds on beaches in New Jersey. Wader Study Group Bulletin, 120, 20-25.

Burger, J., Niles, L., 2014. Effects on five species of shorebirds of experimental closure of a beach in New Jersey: implications for severe storms and sea level rise. Journal of Toxicology

EP

and Environmental Health, 77, 1102-1113.

AC C

Burger, J., Howe, M.A., Hahn, D.D., Chase, J., 1977. Effects of tide cycles on habitat selection and habitat partitioning by migrating shorebirds. Auk, 94, 743-758.

Burger, J., Niles, L., Clark, K.E., 1997. Importance of beach, mudflat and marsh habitats to migrant shorebirds on Delaware Bay. Biological Conservation, 79, 283-292.

22

ACCEPTED MANUSCRIPT

Burger, J., Jeitner, C., Clark, K., Niles, L., 2004. The effect of human activities on migrant shorebirds: Successful adaptive management. Environmental Conservation, 31, 283-288.

RI PT

Burger, J., Carlucci, S.A., Jeitner, C.W., Niles, L., 2007. Habitat choice, disturbance, and

management of foraging shorebirds and gulls at a migratory stopover. Journal of Coastal Research,

SC

23, 1159-1166.

Burger, J., Niles, L., Dey, A.D., Dillingham, T., Gates, A.S., Smith, J., 2015. An experiment to

M AN U

examine how Red Knots Calidris canutus rufa and other shorebirds respond to oyster culture at Reed’s Beach, Delaware Bay, New Jersey. Wader Study Group Bulletin, 122, 89-98.

Butler, R.W., Davidson, N.C., Morrison, R.I.G., 2001. Global-scale shorebird distribution in

TE D

relation to productivity of near-shore ocean waters. Waterbirds, 24, 224-232.

Castel, J., Labourg, P.J., Escaravage, V., Auby, I., Garcia, M.E., 1989. Influence of seagrass beds

EP

and oyster parks on the abundance and biomass patterns of meio- and macrobenthos in tidal flats.

AC C

Estuarine, Coastal and Shelf Science, 28, 71-85.

Conklin, J.R., Battley, P.F., Potter, M.A., Fox, J.W., 2010. Breeding latitude drives individual schedules in a trans-hemispheric migrant bird. Nature Communications, 1, 67.

Connolly, L.M., Colwell, M.A., 2005. Comparative use of longline oyster beds and adjacent tidal flats by waterbirds. Bird Conservation International, 15, 237-266.

23

ACCEPTED MANUSCRIPT

Connors, P.G., Myers, J.P., Connors, C.S.W., Pitekla, F.A., 1981. Intertidal movements of

RI PT

Sanderling in relation to foraging profitability and the tide cycle. Auk, 98, 49-64.

Dey, A.D., Niles, L.J., Sitters, H.P., Kalasz, K., Morrison, R.I.G., 2011. Update to the status of the Red Knot Calidris canutus in the Western Hemisphere, August 2011. Draft update to Status

SC

of the Red Knot (Calidris canutus rufa) in the Western Hemisphere. New Jersey Environmental

M AN U

Protections, unpublished.

Dey, A.D., Niles, L.J., Sitters, H.P., Kalasz, K., Morrison, R.I.G., 2014. Update to the status of the Red Knot Calidris canutus in the Western Hemisphere, August 2014. Draft update to Status of the Red Knot (Calidris canutus rufa) in the Western Hemisphere. New Jersey Environmental

TE D

Department of Environmental Protection, unpublished.

Dill, LM. 2017. Behavioral ecology and marine conservation: a bridge over troubled water?

EP

ICES Journal of Marine Science. Doi:10,1093/icesjms/fsx034.

AC C

Dolman, P.M., Sutherland W.J., 1995. The response of bird populations to habitat loss. Ibis, 137, 538-546.

Dumbauld, B.R., Ruesink J L., Rumrill, S.S., 2009. The ecological role of bivalve shellfish aquaculture in the estuarine environment: a review with application to oyster and clam culture in West Coast (USA) estuaries. Aquaculture. 290, 196-223.

24

ACCEPTED MANUSCRIPT

Federal Register (FR), 2014. Endangered and Threatened Wildlife and Plants; Threatened

[Docket No. FWS–R5–ES–2013–0097; 4500030113

RI PT

Species Status for the Rufa Red Knot. Fish and Wildlife Service, Interior. 50 CFR Part 17

Ferriss, B.E., Reum, J.C.P., McDonald, P.S., Farrell, D.M., Harvey, C.J., 2016. Evaluating

SC

trophic and non-tropic effects of shellfish aquaculture in a coastal estuarine food web. ICES

M AN U

Journal of Marine Science, 73, 429-440.

Galbraith, H., Jones, R., Park, R., Clough, J., Herod-Julius, S., Harrington, B., Page, G., 2005. Global climate change and sea level rise: potential losses of intertidal habitat for shorebirds.

TE D

Waterbirds, 25, 173-183.

Galbraith, H., DesRochers, D.W., Brown, S., Reed, J.M., 2014. Predicting vulnerabilities of

EP

North American shorebirds to climate change. PloS One, 9, e108899.

Gill, J.A., Norris, K., Sutherland, W.J., 2001. Why behavioural responses may not reflect the

AC C

population consequences of human disturbance. Biological Conservation, 97, 265-268.

Gittings, T., O’Donoghue P., 2014. Dungarvan Harbour Special Protection Area: Appropriate assessment intertidal oyster cultivation (including consideration of Helvick Head to Ballyquin SPA and Mid-waterford coast SPA. Unpublished Report prepared by Atkins for the Marine Institute

25

ACCEPTED MANUSCRIPT

Goss‐Custard, J.D., 2014. Birds and people: resolving the conflict on estuaries. Kindle Direct

RI PT

Publishing. E-book available from www.amazon.com.

Goss-Custard, J.D., Triplet, P., Sueur, R., West, A.D., 2006. Critical thresholds of disturbance by

SC

people and raptors in foraging wading birds. Biological Conservation, 127, 88-97.

Harrington, B.A., Loch S., Niles L., Kalasz, K., 2010. Red Knots with different wintering

M AN U

destinations: Differential use of an autumn stopover area. Waterbirds, 33, 357-363.

Hilgerloh, G., O’Halloran, J., Kelly, T.C., Burnell G.M., 2001. A preliminary study on the effects of oyster culturing structures on birds in a sheltered Irish estuary. In Coastal Shellfish—A

TE D

Sustainable Resource. Springer, Netherlands, pp. 175-180.

Intergovernmental Panel on Climate Change (IPCC), 2007. Climate change 2007: synthesis

EP

report. Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate change. Geneva, Switzerland: IPPC.

AC C

https://www.ipcc.ch/pdf/assessment-report/ar4/syr/ar4_syr_full_report.pdf

Intergovernmental Panel on Climate Change (IPCC), 2014. Climate change 2014: impacts, adaptation and vulnerability. Intergovernmental panel on climate change. Geneva, Switzerland: IPPC. https://environmentalmigration.iom.int/climate-change-2014-impacts-adaptation-andvulnerability-contribution-working-group-ii-fifth

26

ACCEPTED MANUSCRIPT

International Wader Study Group (IWSG), 2003. Waders are declining worldwide. Wader

RI PT

Study Group Bulletin 101/102, 8-12.

Kaiser, M.J., Laing, I., Utting, S.D., Burnell, G.M., 1998. Environmental impacts of bivalve

SC

mariculture. Journal of Shellfish Research, 17, 59-66.

Kelly, J.P., Evens, J.G., Stallcup, R.W., Wimpfheimer, D., 1996. Effects of aquaculture on

M AN U

habitat use by wintering shorebirds in Tomales Bay, California. California Fish and Game, 82, 160-174.

Klaassen, M., Lindstrom, A., Meltofte, H., Piersma, T., 2001. Arctic waders are not capital

TE D

breeders. Nature, 413:794.

Kraan, C., van Gils, J.A., Spaans, B., Dekinga, A., Bijteveld, A.L., van Roomen, M., van

EP

Roomen, R., Kleefstra, R., Piersma, T., 2009. Landscape-scale experiment demonstrates that Wadden Sea intertidal flats are used to capacity by molluscivore migrant shorebirds. Journal of

AC C

Animal Ecology, 78, 1259-1268.

Madsen, J., Boertmann D., 2008. Animal behavioural adaptation to changing landscapes: springstaging geese habituate to wind farms. Landscape Ecology, 23, 1007-1011.

27

ACCEPTED MANUSCRIPT

Martín, B., Delgado S., Cruz A.D., Tirado S., Ferrer M., 2015. Effects of human presence on the long‐term trends of migrant and resident shorebirds: evidence of local population declines.

RI PT

Animal Conservation, 18, 73-81.

Mizrahi, D.S., Peters, K.A., Hodgetts, P.A., 2012. Energetic treatments of Semipalmated and Least Sandpipers during northbound migration staging periods in Delaware Bay. Waterbirds, 35,

SC

135-45.

M AN U

Morrison, R.I.G., Hobson, K.A., 2004. Use of body stores in shorebirds after arrival in high Arctic breeding grounds. Auk, 121, 333-344.

Morrison, R.I.G., Aubrey, Y., Butler, R.W., Beyersbergen, G.W., Donaldson, G.M., Gratto-

TE D

Trevor, C.L., Hicklin, P.W., Johnson, V.H., Ross, R.K., 2001. Declines in North American shorebird populations. Wader Study Group Bulletin, 94, 37-42.

EP

Morrison, R.I.G., Davidson, N.C., Wilson, J.R., 2007. Survival of the fittest: body stores on migration and survival in Red Knots, Calidris canutus islandica. Journal of Field Ornithology，

AC C

38，479-487.

Munroe, D., Calvo, L., 2015. Shellfish farmers and restoration scientists finding common ground. Estuary News 25, 8-9.

28

ACCEPTED MANUSCRIPT

Niles, L. J., Sitters, H. P., Dey, A.D., Atkinson, P.W., Baker, A. J., Bennett, K. A., et al., .2008 Status of the Red Knot, Calidris canutus rufa, in the Western Hemisphere. Studies in Avian

RI PT

Biology 36, 1-185.

Niles, L. J., Bart, J., Sitters, H. P., Dey, A. D., Clark, K. E., Atkinson, P. W., et al., 2009. Effects of horseshoe crab harvest in Delaware Bay on Red Knots: are harvest restrictions working?

SC

BioScience 59, 153-164.

M AN U

Daly, D. F., Dillingham, T., Shadel, W., Danihel, M. S., Hafner, S., Wheeler, D., 2013. Restoration of Horseshoe Crab and migratory shorebird habitat on five Delaware Bay beaches damaged by Superstorm Sandy. L.J. Niles Associates, New Jersey.

TE D

Nugues, M. M., Kaiser, M. J., Spencer, B. E., Edwards, D. B., 1996. Benthic community changes associated with intertidal oyster cultivation. Aquaculture Research 27,913-924.

EP

Nisbet, I.C.T., 2000. Disturbance, habituation, and management of waterbird colonies.

AC C

Waterbirds 23, 312-332.

Philippe, A. S., Pinaud, D., Cayatte, M. L., Goulevant, C., Lachaussée, N., Pineau, P., et al., 2016. Influence of environmental gradients on the distribution of benthic resources available for shorebirds on intertidal mudflats of Yves Bay, France. Estuarine, Coastal and Shelf Science. 174, 71-81.

29

ACCEPTED MANUSCRIPT

Piersma, T., Koolhaas, A., Dekinga, A., Beukema, J. J., Dekker, R., Essink, K., 2001. Longterm indirect effects of mechanical cockle-dredging on intertidal bivalve stocks in the Wadden

RI PT

Sea. Journal of Applied Ecology. 38, 976-990.

Piersma, T., Gill, R. E., de Goeij, P. E. T. R. A., Dekinga, A., Shepherd, M. L., Ruthrauff, D., Tibbitts, L., 2006.Shorebird avoidance of nearshore feeding and roosting areas at night correlates

SC

with presence of nocturnal avian predator. Wader Study Group Bulletin 109, 73-75.

M AN U

Pitelka, F. A., 1979. Shorebirds in marine environments. Studies in Avian Biology, No. 2, Allen Press, KS, USA.

Rose, M., Nol, E., 2010. Foraging behavior of non-breeding Semipalmated Plovers. Waterbirds

TE D

33,59-69.

Smit, C. J., Visser, G. J. M., 1993. Effects of disturbance on shorebirds: a summary of existing

EP

knowledge from the Dutch Wadden Sea and Delta area. Wader Study Group Bulletin 68, 6-19.

AC C

Solomon, O.O., Ahmed, O. O., 2016. Ecological consequences of oyster culture: a review. International Journal of Fisheries and Aquatic Studies 4, 1-6.

Spencer, B. E., Kaiser, M. J., Edwards, D. B., 1996. The effect of Manila clam cultivation on an intertidal benthic community: the early cultivation phase. Aquaculture Research 27, 261-276.

30

ACCEPTED MANUSCRIPT

Spencer, B. E., Kaiser, M. J., Edwards, D. B., 1997. Ecological effects of intertidal Manila clam cultivation: observations at the end of the cultivation phase. Journal of Applied Ecology 34,444-

RI PT

452.

Statistical Analysis Systems (SAS), 2005. Statistical Analysis. SAS, Cary, SC, USA.

SC

Stillman, R.A., A. D. West, R. W. G. Caldow, and S. E. A. Durell (2007) Predicting the effect of

M AN U

disturbance on coastal birds. Ibis 149: 73-81.

Subasinghe, R., 2006. State of World Agriculture 2006. FAO Fisheries Technical Paper, Rome, Italy.

TE D

Tarr, N. M., Simons, T. R., Pollock, K. H., 2010. An experimental assessment of vehicle disturbance effects on migratory shorebirds. Journal of Wildlife Management 74, 1776-1783.

EP

Tsipoura, N., Burger, J., 1999. Shorebird diet during spring migration stop-over on Delaware

AC C

Bay. Condor 101, 635–644.

U.S. Fish & Wildlife Service (USFWS). 2016. Programmatic biological assessment for structural shellfish aquaculture projects for Red Knot (Calidris canutus rufa): Lower Delaware Bay, NJ. USFWS,

31

ACCEPTED MANUSCRIPT

van Gils, J. A., Lisovski, S., Lok, T., Meissner, W., Ożarowska, A., de Fouw, J., 2016. Body shrinkage due to Arctic warming reduces Red Knot fitness in tropical wintering range. Science

RI PT

352, 819-821.

Warnock, N., Elphick, C., Rubega, M.A., 2002. Shorebirds in the marine environment. In:

SC

Schreiber, B.A., Burger, J. (Eds.), Biology of marine birds. CRC Press, FL, USA, pp. 582-655.

Yasue, M., 2005. The effects of human presence, flock size and prey density on shorebird

AC C

EP

TE D

M AN U

foraging rates. Journal of Ethology 23, 199-204.

32

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

33

ACCEPTED MANUSCRIPT

Table 1. Number of shorebirds observed in May 2013 and 2016 for the experiment testing the effects of oyster racks, reefs and controls (analysis includes censuses with zero shorebirds present) at Reed’s Beach, New Jersey (USA). Note that the reefs were established over a year

RI PT

before the oyster racks were built. Given is Kruskal-Wallis non-parametric ANOVA.

% of censuses

Mean (includes Zeros)

SC

with some shorebirds present

All Shorebirds 2013 (N = 279) 73.9%

Controls

48.3%

X2 (p) 2016 (N = 231)

+

63.7

4360

245.6

+

70.9

7800

14.2 (0.0002)

78.4%

368.4

±

40.7

3750

70.3%

244.5

±

31.6

2725

Oyster racks

68.7%

89.3

±

9.8

920

Control

74.9%

303.8

±

32.1

2305

AC C

1 reef

EP

2 reefs

Max

320.8

TE D

Oyster racks

Std Error

M AN U

Treatment

X2 (p)

46.4 (<0.0001)

Foraging Shorebirds 2 reefs

78.4%

320.5

±

37.6

3450

1 reef

69.9%

211.7

±

28.8

2525

ACCEPTED MANUSCRIPT

Oyster racks

67.0%

74.6

Control

74.5%

248.3

X2 (p)

±

7.9

700

27.9

2100

Roosting Shorebirds 27.7%

47.9

±

7.1

1 reef

26.6%

32.8

±

5.8

Oyster racks

22.6%

14.7

±

2.9

Control

37.7%

55.5

±

X2 (p)

SC

2 reefs

RI PT

47.2 (<0.0001)

7.4

AC C

EP

TE D

M AN U

17.6 (0.0005)

600 783 225 760

ACCEPTED MANUSCRIPT

a. Only censuses are included when there were other shorebirds present; in this case zeros

AC C

EP

TE D

M AN U

SC

RI PT

means no knots were present, but other shorebirds were present.

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

ACCEPTED MANUSCRIPT

Table 2. Total number of Red Knots observed during the 2013 and 2016 experiments at Reeds Beach. Data includes only observations when any shorebird was present. Given are Kruskal-Wallis non-parametric ANOVA from SAS PROC NPAR1WAY.

RI PT

Mean Red Knots

(includes Zeros)a % of Obs with Red Knots present

All Red Knots

M AN U

2013

Std Error

SC

Treatment

Max

Oyster racks

13.1%

13.0 ±

4.9

360

Control

16.8%

58.6 ±

23.2

1500

X2 (p)

TE D

2016 2 reefs

53.0%

78.2 ±

14.1

1130

44.5%

67.5 ±

15.6

1315

34.0%

12.6 ±

2.8

235

48.0%

79.9 ±

13.1

1175

AC C

Control

EP

1 reef Oyster racks

7.2 (0.007)

X2 (p)

24.2 (<0.0001)

Foraging Red Knots (2016)

2 reefs

53.0%

71.6 ±

12.7

880

1 reef

44.5%

64.1 ±

15

1250

Oyster racks

33.0%

12.3 ±

2.8

235

ACCEPTED MANUSCRIPT

Control

48.0% X2 (p)

70.3 ±

11.5

925

25.5 (<0.0001)

Roosting Red Knots

RI PT

(2016) 12.5%

6.6

±

2.3

250

1 reef

8.5%

3.3

±

1.1

150

Oyster racks

3.0%

0.3

±

0.1

20

Control

9.5%

9.6

±

2.8

250

12.6 (0.006)

M AN U

X2 (p)

SC

2 reefs

a. Only censuses are included when there were other shorebirds present; in this case zeros

AC C

EP

TE D

means no knots were present, but other shorebirds were present.

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

ACCEPTED MANUSCRIPT

Table 3. Models (SAS, Proc GLM) explaining differences in the number of all shorebirds present, and the number of Red Knots present when other shorebirds were present. The experiments at Reeds Beach South (New Jersey, USA) in 2013 included only oyster racks and

RI PT

control, and in 2016 included artificial reefs, racks, and control site. The treatments in 2016 were adjacent to one another, and separated by fences that extended out into the water farther

2013 Total

2016 Total

Shorebirds

Shorebirds

Model 6.8

P

<0.0001

Df

32

R2

0.47

Independent variables

Knots

Red Knots

10.1

6.1

24.9

<0.0001

<0.0001

<0.0001

54

33

54

0.40

0.60

0.69

NS

15.8 (<0.0001)

11.4 (0.001)

7.2 (<0.0001)

Tide time

NS

11.1 (0.0009)

NS

NS

10.2 (<0.0001)

23.6 (<0.0001)

NS

8.3 (<0.0001)

NS

13.5 (0.0003)

NS

NS

2.7 (0.001)

2.2 (<0.0001)

2.2 (0.01)

NS

Not applicable

Not applicable

79.7 (<0.0001)

650 (<0.0001)

AC C

Treatment

EP

F(p)

2016 Total

TE D

F

2013 Total Red

M AN U

Model

SC

than the exposed intertidal flats. NS = not significant.

Date

Time of day

Treatment X Date Number of non-Knot shorebirds

ACCEPTED MANUSCRIPT

Number of Laughing

17.1 (<0.0001)

NS

NS

NS

AC C

EP

TE D

M AN U

SC

RI PT

Gulls

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

Figure 4