Population Statistics (ESP 121, Winter 2020) Term Paper

Ecological Drivers of the Delaware Bay Red Knot Population: Trends from 1971-present.
Connor Heuerman and Elisa Fernandes-McDade

Photo: Gregory Breese/USFWS (2009)

Species: Red Knot (Calidris canutus)
Main ID: 11
Taxon ID: 10
Time Series: 1970-1992
Generation Length: 6.8 years

Introduction
The Red Knot (Calidris canutus) is one of the planet’s most prolific flyers; it has one of the
longest migration routes in the animal kingdom. It is a long-distance migratory shorebird which
travels up to 30,000 kilometers a year, breeding in the high Arctic, and wintering on subarctic
coasts from Ireland down to the southernmost tip of South America (Delaware Riverkeeper
Network, 2005; BirdLife International, 2018). Red Knots primarily consume marine
invertebrates during non-breeding season and eat the eggs of Horseshoe crabs during spring
migration (Baker et al., 2013). Its migratory nature means that this species is dependent upon
suitable habitat and sufficient prey in breeding, non-breeding, and migration stopover habitat.
Like many migratory shorebirds, it is vulnerable to coastal development, habitat loss due to sea
level rise, human disturbance, and decreases in marine invertebrate populations (Andres et al.,
2012; Martín et al., 2014). Recent estimates suggest that the Red Knot, though widespread, is
declining worldwide. This is significant as Red Knots provide value not only through the means
of ecotourism, but also through their role of being invertebrate consumers in various global
coastal food webs and excellent indicators of coastal ecosystem conditions (Niles et al., 2008).
This paper will investigate ecological drivers behind the population trends of the nearctic
subspecies of Red Knot, the Delaware Red Knot, (Calidris canutus rufa) inhabiting the eastern
coasts of the Americas and high Arctic, a population which is notable in academic literature for
being dependent on Horseshoe crab (Limulus polyphemus) spawning events on migration
(McGowan et al., 2011).

Figure 1: Red Knot population trend is negative from 1971-1991 (Prys-Jones, 1994).

The Red Knot population between 1971-1991 trends downward over the 20 year period. In the
first eight years the population sees a significant decline from as high as 127,000 in 1972 to as
low as 58,500 in 1978. The population then partially increases/recovers for a span of five years
reaching 80,000 in 1983, then fluctuates within a difference of approximately 15,000 individuals
for the remainder of the series.

Current Status
As of 2018, the Red Knot is classified as Near Threatened and Declining by the IUCN (BirdLife
International, 2018). The total global population according to the most recent, reliable data is
estimated to be between 891,000-979,000 individuals, while the focal subspecies population is
estimated to be between 27,000-30,000 individuals. This number, based on counts from
long-term surveys in Delaware Bay and Tierra del Fuego, represents a precipitous 37% decline
since 1997 (Baker et al., 2004; Smith et al., 2016). This subspecies is highly sensitive to changes
in the timing and abundance of Horseshoe Crab populations in Delaware Bay and
strategically-spaced stopover habitat on the east coast of the United States.

Predator-Prey Dynamics: Horseshoe Crabs

The American Horseshoe Crabs is a 200 million year old marine arthropod species that inhabits
the Atlantic coast from New York to Florida (Walls et al., 2002). Adults winter in cold offshore
waters and breed on sandy beaches from March to July. The most dramatic spawning event--and
the most important for Red Knots--takes place from May to June in Delaware Bay, triggered by a
new moon and full moon tide. Delaware Red Knots are unique in that they are reliant on
consuming Horseshoe Crab eggs in the Delaware Bay en route to Arctic breeding grounds. These
Red Knots must achieve both the goal of reaching Delaware Bay at the peak of egg laying and
reaching the threshold body mass of 180-200 g in order to cover the energy costs/warmth needed
for the journey (Baker et al., 2004). Failing to achieve both of these goals can be fatal.
For management purposes, Horseshoe Crabs can be considered a multiple-use resource in
Delaware Bay, utilized by wild animals and multiple fisheries. Delaware Bay Red Knots
compete with Dunlins (Calidris canutus), Ruddy Turnstones (Arenaria interpres), Sanderlings
(Calidris alba), and other shorebird species for eggs. The totality of migrating shorebirds in
Delaware Bay consume roughly 539 metric tons of eggs over the laying period, largely to
increase body mass before completing the last legs of migration to the Arctic (Castro and Myers,
1993). The caloric value of Horseshoe Crab eggs to migrating birds cannot be understated.
Knots have also faced competition from human fisheries which have been harvesting
Horseshoe Crab adults since the 1990s for biomedical purposes and for eel and whelk bait..
Currently, biomedical fisheries practice a capture and release method for harvesting the cloudy
blue blood of adult Horseshoe Crabs, which is used to synthesize Limulus Amebocyte Lysate
(LAL), a clotting agent used in vaccines and endotoxin detection devices (Krisfalusi-Gannon et
al, 2018; Leschen and Correia, 2010). Researchers and environmentalists have recently raised
concerns that biomedical harvest may be unsustainable on account of poor record keeping by
bleeders, a complete lack of
regulation on the amount of
allowable blood extraction, and the
physiological effects on released
crabs. The biomedical harvest is a
cause of direct and indirect
mortality. Industry-provided
estimates place direct mortality rates
from harvest at about 10-30% or
130,000 crabs annually (Maloney et
al., 2018). Tracking studies have
shown that being captured causes
disorientation in both control and
bled groups, but the bled group
showed less-directional movement
patterns for a longer period and
experienced a 15-30% mortality rate
within two weeks of being bled
(Kurz and James-Pirri, 2010). It
should be noted that the tracking
studies which mimicked industry
standard

Figure 2: Atlantic States Marine Fisheries Commission (n.d.)

handling strongly suggested that direct-cause mortality can be largely attributed to the stress and
hypoxic conditions of conventional methods rather than bleeding exclusively.
Human harvest increased total crab mortality by 75% and decreased spawning
populations by 95% in some areas since the 1990s (Atlantic States Marine Fisheries
Commission, 2013; Widener and Barlow, 1999). One count in Cape Cod recorded a staggering
decline of spawning crabs from 3,000 individuals in 1984 to 148 individuals in 1999. Annual
records from the Atlantic States Marine Fisheries Commission report that 20,000 more crabs
were killed during harvest each year since 2007 than are allowable by the Commission. Statistics
from commercial bait landings and biomedical harvest along the American Northeast show a
distinct decline and implicate anthropogenic predation as the primary cause.
Empirical data support the idea that the onset of crab harvest coincided with the decline
of Delaware Bay Red Knots. Horseshoe Crab populations have stagnated far below pre-harvest
levels since 2005 and Red Knots have responded in kind (U.S. Fish and Wildlife Service, 2015).
Select studies warn that the crab harvest precipitated a trophic cascade that acutely impacted
shorebirds. There is consensus in fisheries literature that overexploitation--particularly of female
adults--in multispecies systems can lead to trophic cascade, an outcome borne out by
mathematical models and observational studies (Anderson and Pederson, 2009; Beddington and
May, 1980; Daskalov, 2002). Determining maximum sustainable yield is difficult in a healthy
fishery, let alone one that is decidedly in decline, as is the case in Delaware Bay. The following
equations are adapted from the Beddington and May (1980) model of a sperm whale, squid, and
krill fishery. First, a Lotka-Volterra model is used to determine a single predator’s exploitation of
the prey species:
Prey:
𝑑𝑁1
𝑑𝑡
= 𝑟1𝑁1 1 − ( 𝑁1
𝐾 ) − 𝑎𝑁 𝑁
1 2
𝑑𝑁 𝑁
Predator: = 𝑟2𝑁 2⎡⎢1 − α𝑁 2 ⎤⎥
𝑑𝑡
2

⎣ 1 ⎦

Predator growth (𝑟2) is directly proportional to prey abundance (α).

The model is then scaled and non-dimensionalized. The original model accounts for both
predator and prey being harvested. Here, only the non-dimensionalized prey model will be
featured to represent Horseshoe crab harvest.
𝑎α𝐾
New parameters: v = 𝑟 ;𝑌1=𝑟1𝐹1𝑋1= yield of prey; 𝐹1 = 1 = 𝑟1
1
𝑑𝑋1
Equilibrium: 𝑑𝑡
= 0
MSY: v = 1 results when predator harvests prey at maximum sustainable yield, v > 1
results when predator harvest exceeds MSY, and v < 1 results when harvest is less than MSY.
𝑑𝑋1
Prey: 𝑑𝑡
= 𝑟1𝑥1(1 − 𝑋1 − 𝑣𝑋2) − 𝑌1
𝑑𝑋1
Prey w/ fishing effort: 𝑑𝑡
= 𝑟1𝑋1(1 − 𝐹1 − 𝑋 − 𝑣𝑋2). This model would be
1
appropriate for evaluating the predator-prey dynamic for Red Knots and Horseshoe Crabs under
increasing fishing efforts (𝐹1) and due to Red Knot predation alone (i.e. evaluating v).
An expanded model accounts for the dynamics between a harvested prey species, a
harvested predator species, and a competing predator that is not harvested. The following model
would be appropriate for evaluating the dynamic between Horseshoe Crabs (harvested prey),
loggerhead turtles (harvested marine predator), and Red Knots (unharvested competing predator;
predation on Horseshoe Crab would be represented byμ).
𝑑𝑋1
Harvested prey: 𝑑𝑡
= 𝑟1𝑋1(1 − 𝑋1 − 𝑣𝑋2 − μ𝑋3) −𝑌1
𝑑𝑋2 𝑋2
Harvested predator: 𝑑𝑡
= 𝑟2𝑋2(1 − 𝑋1
) −𝑌1
𝑑𝑋3 𝑋3
Unharvested predator: 𝑑𝑡
= 𝑟3𝑋3(1 − 𝑋1
)
 𝑣
Non-dimensionalized parameters: v’ = 1+μ

Non-dimensionalized model: 𝑌'1 = 𝑟1𝑋'1 (1 − 𝑋'1 − 𝑣'𝑋'2 )

𝑋'2
𝑌'2 = 𝑟2𝑋'2 (1 − )
𝑋'1

An even more comprehensive model encompassing multiple trophic levels in a

multispecies fishery was proposed by Walter et al. (1997), which would be appropriate for a
holistic assessment of Horseshoe Crab trends in the context of the entire Delaware Bay fishery.
The Walter et al. model accounts for both mortality by anthropological (𝐹𝑖) and natural causes (
𝑀𝑖), in addition to total multi-species predation (Σ𝐶𝑗𝑖).
𝑑𝐵𝑖
𝑑𝑡
= 𝑔𝑖Σ𝐶𝑗𝑖 − Σ𝐶𝑗𝑖 − 𝐼𝑖(𝑀𝑖 + 𝐹𝑖 + 𝐸𝑖)𝐵𝑖
Both the Beddington and May and Walter et al. models are broadly applicable to
predator-prey dynamics with harvest pressure on the prey side. However, Red Knots and
Horseshoe Crabs are subject to species-specific ecological and anthropological drivers
necessitating predator-prey models with specialized parameters on the predator side and prey
side. Multiple models have been proposed to address this need. One model developed during the
2007 USFWS Structured-Decision Making Workshop incorporated female Horseshoe Crab
𝐻𝑆𝐶 𝐴𝑑𝑅𝐾
abundance(𝑁𝑡 ), female crab harvest (𝐻𝑡), early-arrival adult Red Knot abundance (𝑁𝑡 ),
𝐸𝐺𝐺𝑆
number of eggs accessible to Knots (𝑁𝑡 ), and adult Red Knot survival and reproduction as a
function of sufficient body mass at the time of departure from Delaware Bay (𝑃180) (Breese et
al., 2007).
𝐻𝑆𝐶 𝐻𝑆𝐶
Female Horseshoe Crab abundance: 𝑁𝑡+1 = 𝑁𝑡 + 𝑓(𝐻𝑡)
𝐴𝑑𝑅𝐾 𝐴𝑑𝑅𝐾
Early-arrival adult Red Knot abundance: 𝑁𝑡+1 =𝑁𝑡 + 𝑓(𝑃180,𝑡)
𝐸𝐺𝐺𝑆 𝐻𝑆𝐶
Number of Red Knot-accessible eggs: 𝑁𝑡 =𝑓(𝑁𝑡 )
𝐸𝐺𝐺𝑆
Red Knots survival/reproduction as a function of weight: 𝑃180,𝑡 = 𝑓(𝑁𝑡 )

Migration Timing and Stopover Sites

The global ailments to this cosmopolitan species are threats to its littoral habitat such as coastal
development, disturbance due to seasonal disturbance, toxic effluents, habitat change, and sea
level rise. Long-distance migrants like the Delaware Bay Red Knot are dependent on a handful
of highly productive sites for rest and refueling over the course of their migration. This high site
fidelity makes them extremely vulnerable to habitat change because they are already physically
exhausted upon arrival, and are generally unable to suddenly adjust migration patterns if the
species’ destinations have been altered beyond suitability or removed entirely since the last
migration. Additionally, recent large-scale studies of North American and Eurasian long- and
short-distance migrants suggest that long-distance migrants may also miss peak prey abundance
at stopover and breeding sites when asynchronous temperature cues in their non-breeding sites
prompt mistimed migration (Both et al., 2006; Zaifman et al., 2017). The sheer distance between
sites in South America and North America results in an inability to detect physical changes to
stopover sites and changes to Horseshoe Crab egg laying timing prior to departure.
A model developed by Berestycki et al. (2008) proposes that a species’ ability to react to
climate change can be evaluated by adapting the following reaction-diffusion model:
2
∂𝑢 ∂𝑢
∂𝑡
= 𝐷 2 + 𝑓(𝑢, 𝑥 − 𝑐𝑡)
∂𝑥
c = 0 before climate change and c > 0 after climate change, u = population
density, D = dispersal constant independent of climate, f = net population growth
as a function of climate suitability.
Currently, several factors are threatening the health of the stopover sites in both Delaware
Bay and Tierra del Fuego. In South America, the primary threat to stopover sites is from oil
pollution. However, there have been no observed incidences of oil contamination of food sources
affecting Red Knot stopover sites (Niles et al., 2008). As previously mentioned, the most serious
threat to the Delaware Bay stopover site is the reduction in the amount of Horseshoe Crab eggs
available for the Red Knots to consume. According to Niles et. al., several factors worsen this
situation, namely beach erosion, human and dog disturbance, and interference competition from
gulls.
Sea level rise and increasing storm intensity as a result of climate change also exacerbate
the rate of beach erosion, leading to the destruction of intertidal and crab-spawning habitat. Red
Knots rely on low tides to gain access to soft-bodied invertebrates on migration and on their
breeding grounds. In the Arctic, foraging in suboptimal habitat and increased search time (i.e.
more time spent flying between patches) for optimal habitat is directly correlated with reduced
body mass (van Gils et al., 2004). Sea levels are predicted to rise on the east coast of the
northeastern United States, which will likely reduce the utility of stopover sites (Gornitz, 1990).
The presence of humans and dogs reduces the already limited amount of feeding time
Red Knots have during migration and can prevent the birds from feeding at optimal sites, as
human/dog disturbance often causes them to fly away. Gulls are more tolerant of both human and
dog disturbances than Red Knots, and serve as competitors for food and potential predators of
Red Knots (Niles et al. 2008). A study conducted by Hernandez (2005) found that the presence
of gulls in stopover sites reduced the Red Knot’s foraging efficiency by as much as 40%. The
greater the presence of one or more of these species reduces the utility of otherwise suitable
habitat.

Predator-Prey Dynamics: Lemmings

In addition to their link with Horseshoe Crabs, studies have explored the possibility of lemmings
being a potential driver of the decline of the rufa Red Knot subspecies. Analysis completed by
Fraser et al. (2013), suggests that the population dynamics of the rufa Red Knot subspecies may
be driven by pressure exerted by native lemming-predator cycles. Historically, other Red Knot
subspecies’ population declines have correlated with declines in lemming populations due to
foxes beginning to prey on more shorebirds once lemmings become scarce (Fraser et al., 2013).
Therefore, a sharp increase in lemming population would correspond with an increase in the
reproductive output of the rufa red subspecies.
Researchers used data collected from Delaware Bay from 1986 to 1998; the data
documented the weekly counts of the Red Knots during their migration and detailed rodent
population numbers during the same time period. In order to see lemming increases
corresponded with Red Knot increases, researchers used a fourier model, which measures
periodicity by deconstructing more complex
waves into sine and cosine waves.

(Figure 3: Highest annual counts of Red Knots in

Delaware bay from 1982 to 2006 vs. Rodent cycle
peak vs non-peak from 1984 to 2006 Fraser et al.,
2006 )

These resulting sine and cosine waves can be used

to see if the rufa Red Knot species declines occur
at intervals that align with native lemming
population peaks. The researchers hypothesized
that if a connection between the two populations
existed, Red Knot population peaks would come
two years after lemming population peaks (Fraser
et al., 2013). The researchers found that before
each of the four observed Red Knot population peaks, lemming populations were either
increasing or had peaked two years prior (Fraser et al., 2013). This finding is consistent with the
hypothesis that the native lemming population is a driver of Delaware Bay Red Knot dynamics.
It is important to note that this study was limited by many factors. The data on Delaware
Bay Red Knots was an incomplete count, as the data was collected on a weekly rather than a
daily basis. This allows for the possibility of peak numbers of the Delaware Bay Red Knot to
occur on days in which there was no data collection. Additionally, specific lemming data was not
available for the analysis, the researchers relied on general rodent population statistics for the
region during the specified time period (Fraser et al., 2013). The limitations of the data do not
allow for a concrete answer on whether lemming population cycles are a driver for the declining
rufa Red Knot subspecies. However, these findings support the potential for a linkage between
the two populations; further research needs to be conducted in order to truly see how lemming
population cycles affects the Red Knot’s population dynamics.

Discussion
Migratory shorebirds are integral members of the ecosystems in which they inhabit. Shorebirds
consume large amounts of invertebrates in coastal food webs, which helps to stabilize coastal
food webs. They also maintain an important role in both nutrient cycling and seed dispersal: the
birds disperse both food remains and seeds in each habitat they migrate to, which in turn
positively affects the growth of plants in those ecosystems (Great Barrier Reef Marine Park
Authority, 2012). Shorebird droppings (guano) also play an important role in ecosystems, as the
guano fertilizes both the water and land ecosystems, which increases productivity (Warnock et
al., 2002). Shorebirds possess the ability to cover great distances around the world during their
annual migrations, an ability making them valuable to humans from both a cultural and practical
standpoint. Shorebirds’ unique globe-trotting ability inspire conservation efforts to protect the
species as they can provide potential aesthetic, recreational, and economic value. Additionally,
analyzing the population dynamics of shorebirds allows scientists to gauge the effects of climate
change, as studying the factors affecting shorebird populations also serves as an indicator for the
factors driving climate change due to shorebirds’ global presence (Galbraith et al., 2014).
Red Knot populations are in serious danger of extinction without immediate management
intervention. Given that the lack of Horseshoe Crab eggs is the primary driver of declining Red
Knot populations, actions to increase the availability of these eggs should be pursued to recover
the population. As of 2018, a synthetic crab blood substitute has been synthesized which will
likely curb harvest pressure and cause a bottom-up effect on Red Knots (Maloney et al., 2018).
Legislation should be passed to protect the Delaware Bay stopover site from repeated
disturbances from humans and dogs. Additionally, long-term solutions for curtailing gull
competition with Red Knots over Horseshoe Crab eggs should be explored. Further analysis
regarding the potential of lemming populations as a secondary driver should be completed to
fully understand all potential drivers and their subsequent impacts on Red Knot population
dynamics. Addressing each driver of Red Knot populations as soon as possible will help secure
the long-term survival of this species.

Citations
1. Anderson K.H. and Pederson M. (2009). Damped trophic cascades driven by fishing in
model marine ecosystems. Proceedings of the Royal Society B, 277(1682).
https://doi.org/10.1098/rspb.2009.1512.
2. Andres B.A., Smith P.A., Morrison R.I.G., Gratto-Trevor C.L., Brown S.C. & Friis C.A.
(2012). Population estimates of North American shorebirds, 2012. Wader Study Group
Bulletin, 119(3): 178–194.
3. Atlantic States Marine Fisheries Commision. (2013). 2013 Horseshoe Crab Stock
Assessment Update. Prepared by the Sweka J.A., Klopfer M., Millard M., Olszewski S.,
Smith D., Sysak R., and Wong R. [PDF] Accessed from
http://www.asmfc.org/uploads/file//52a88db82013HSC_StockAssessmentUpdate.pdf.
4. Atlantic States Marine Fisheries Commission. (n.d.) Horseshoe Crab Bait Landings and
Biomedical Collection. [Photograph] Accessed March 12, 2020 from
http://www.asmfc.org/species/Horseshoe-crab.
5. Baker A. J., González P.M., Piersma T., Niles L.J., do Nascimento I. de L.S., Atkinson
P.W., Clark N.C., Minton C.D.T., Peck M.K., and Aarts G. (2004). Rapid population
decline in Red Knots: Fitness consequences of decreased refueling rates and late arrival
in Delaware Bay. Proceedings of the Royal Society of London, Series B (271): 875-882.
6. Baker A., Gonzalez P., Harrington B. A., and Morrison R. I. G. (2013). Red Knot.
Retrieved February 28, 2020 from
https://birdsna.org/Species-Account/bna/species/redkno/introduction/.
7. Beddington J.R. and May R.M. (1980). Maximum Sustainable Yields in Systems Subject
to Harvesting at More Than One Trophic Level. Mathematical Biosciences, 51(3-4):
261-281. https://doi.org/10.1016/0025-5564(80)90103-0.
8. Berestycki H., Diekmann O., Nagelkerke C.J., and Zegeling P.A. (2009). Can a Species
Keep Pace with a Shifting Climate? Bulletin of Mathematical Biology, 71(399).
https://doi.org/10.1007/s11538-008-9367-5.
9. BirdLife International 2018. Calidris canutus . The IUCN Red List of Threatened Species
2018: e.T22693363A132285482.
https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22693363A132285482.en.
Downloaded on March 01, 2020.
10. Both C., Bouwhuis S., Lessells C.M., and Visser M.E. (2006). Climate change and
population declines in a long-distance migratory bird. Nature, 441: 81-83.
11. Breese G., USFWS (2009). Red knot feeding on Horseshoe crab eggs in Delaware Bay.
[Photograph] Retrieved March 12, 2020 from
https://www.flickr.com/photos/usfwsnortheast/4035465562/sizes/o/in/set-7215762251677
2109/.
12. Breese G., Smith D., Nichols J., Lyons J., Hecht A., Clark N., Michels S., Millard M.,
Scherer A., Spear B., Brewer D.C., Starfield A.M., and Runge M.C. (2007). Application
of Structured Decision Making to Multi-Species Management of Horseshoe Crab and
Shorebird Populations in Delaware Bay. 2007 Structured Decision Making Workshop,
9-13 July 2007. National Conservation Training Center, Shepherdstown, WV, USA.
Accessed March 11, 2020 from
https://www.researchgate.net/profile/Gregory_Breese/publication/267970114_2007_Struc
tured_Decision_Making_Workshop_Application_of_Structured_Decision_Making_to_M
ulti-Species_Management_of_Horseshoe_Crab_and_Shorebird_Populations_in_Delawar
e_Bay/links/54b7c1310cf2bd04be33c765/2007-Structured-Decision-Making-Workshop-
Application-of-Structured-Decision-Making-to-Multi-Species-Management-of-Horsesho
e-Crab-and-Shorebird-Populations-in-Delaware-Bay.pdf
13. Daskalov G.M. (2002). Overfishing drives a trophic cascade in the Black Sea. MEPS,
225: 53-63. doi:10.3354/meps225053.
14. Delaware Riverkeeper Network, American Littoral Society, Delmarva Ornithological
Society, Delaware Chapter of the Sierra Club, and New Jersey Audubon Society. 2005.
Petition to List the Red Knot (Caladris canutus rufa) as Endangered and request for
Emergency Listing under the Endangered Species Act. [PDF] Accessed February 28,
2020 from https://www.fws.gov/northeast/redknot/riverkeeper.pdf
15. Fraser J.D., Karpanty S.M., Cohen J.B., & Truitt B.R. (2013). The Red Knot (Calidris
canutus rufa) decline in the western hemisphere: is there a lemming connection?
Canadian Journal of Zoology, 91(1), 13-16.
16. Galbraith H., DesRochers D.W., Brown S., and Reed J.M. (2014). Predicting
vulnerabilities of North American shorebirds to climate change. PloS One, 9(9).
17. Gornitz V. (1990). Vulnerability of the East Coast, U.S.A. to Future Sea Level Rise.
Journal of Coastal Research, 201-237. Retrieved March 12, 2020, from
www.jstor.org/stable/44868636.
18. Great Barrier Reef Marine Park Authority. (2012). A vulnerability assessment for the
Great Barrier Reef: Offshore and foraging pelagic seabirds. Accessed March 11, 2020
from
http://elibrary.gbrmpa.gov.au/jspui/bitstream/11017/2950/1/gbrmpa-VA-OffshorePelagicS
eabirds-11-7-12.pdf.
19. Hernandez D. E. (2005). Conservation and foraging dynamics of migratory shorebirds
(Doctoral dissertation, Rutgers The State University of New Jersey-New Brunswick).
20. Kurz W. and James-Pirri M.W. (2010). The impact of Biomedical Bleeding on Horseshoe
Crab, Limulus polyphemus, Movement Patterns on Cape Cod, Massachusetts. Marine
and Freshwater Behaviour and Physiology, 35(4).
https://doi.org/10.1080/1023624021000019315.
21. Krisfalusi-Gannon J., Ali W., Dellinger K., Robertson, L., Brady T.E., Goddard M.K.M.,
Tinker-Kulberg R., Kepley C.L. and Dellinger A.L. (2018). The Role of Horseshoe Crabs
in the Biomedical Industry and Recent Trends Impacting Species Sustainability. Frontiers
in Marine Science, 5: 185. doi: 10.3389/fmars.2018.00185.
22. Leschen A.S. and Correia S.J. (2010). Mortality in female Horseshoe crabs (Limulus
polyphemus) from biomedical bleeding and handling: implications for fisheries
management. Marine and Freshwater Behaviour and Physiology, 43(2): 135-147.
23. Maloney T., Phelan R., Simmons N. (2018) Saving the Horseshoe crab: A synthetic
alternative to Horseshoe crab blood for endotoxin detection. PLoS Biology, 16(10):
e2006607. https://doi.org/10.1371/journal.pbio.2006607
24. Martín B., Delgado S., de la Cruz A., Tirado S., and Ferrer M. (2014). Effects of human
presence on the long-term trends of migrant and resident shorebirds: evidence of local
population declines. Animal Conservation, 18(1): 73-81.
https://doi.org/10.1111/acv.12139.
25. Niles L. J., Sitters H. P., Dey A. D., Atkinson P. W., Baker A. J., Bennett K. A., and
González, P. M. (2008). Status of the Red Knot (Calidris canutus rufa) in the Western
Hemisphere. In Status of the Red Knot (Calidris Canutus Rufa) in the Western
Hemisphere (pp. 1-185). Accessed March 12, 2020 from
https://sora.unm.edu/sites/default/files/journals/sab/sab_036.pdf.
26. Prys-Jones R.P., Underhill L.G., and Waters R.J. (1994). Index Numbers for Waterbird
Populations. II. Coastal Wintering Waders in the United Kingdom, 1970/71-1990/91.
Journal of applied ecology: 481-492.
27. Smith F.M.,Watts B.D., Lyons J.E., and Keyes T.S. (2016). Investigating Population
Dynamics of Red Knot Migration along the Georgia Coast through Mark/Recapture
Analysis of Resights: Spring 2015 Season. Center for Conservation Biology Technical
Report Series, CCBTR-16-05. College of William and Mary/Virginia Commonwealth
University, Williamsburg, VA. 13 pp.
28. U.S. Fish and Wildlife Service. (2015). Status of the species -- Red Knot (Calidris
canutus rufa).
https://www.fws.gov/verobeach/StatusoftheSpecies/20151104_SOS_RedKnot.pdf
29. Van Gils J.A., Dekinga A., Spaans B., Vahl W.K., and Piersma T. (2004). Digestive
bottleneck affects foraging decisions in Red Knots Calidris canutus. II. Patch choice and
length of working day. Journal of Animal Ecology, 74(1): 120-130.
https://doi.org/10.1111/j.1365-2656.2004.00904.x.
30. Walls E.A., Jim B., and Smith S.A. (2002). The Horseshoe Crab, Limulus polyphemus:
200 Million Years of Existence, 100 Years of Study. Reviews in Fisheries Science, 10:1,
39-73, DOI: 10.1080/20026491051677.
31. Walters C., Christensen V. & Pauly D. Structuring dynamic models of exploited
ecosystems from trophic mass-balance assessments. Reviews in Fish Biology and
Fisheries 7, 139–172 (1997). https://doi.org/10.1023/A:1018479526149.
32. Warnock N., Elphick C., Rubega M.A. (2002). Shorebirds in the marine environment. In:
Schreiber EA, Burger J, editors. Biology of marine birds. Boca Raton: CRC Press. pp.
581–615
33. Widener J.W. and Barlow R.B. (1990). Decline of a Horseshoe Crab Population on Cape
Cod. The Biological Bulletin 197, 2: 300-302. https://doi.org/10.2307/1542664.
34. Zaifman J., Shan D., Ay A., and Jimenez A.G. (2017). Shifts in Bird Migration Timing in
North American Long-Distance and Short-Distance Migrants Are Associated with
Climate Change. International Journal of Zoology, Article ID 6025646, 9 pages
https://doi.org/10.1155/2017/6025646.