Pre-meeting background material for the 2011 International Workshop on the Science and Conservation of Asian Horseshoe Crabs (13-16 June 2011, Hong Kong, China] Carl N. Shuster Jr.

NOTE: Because I will not be able to attend the workshop, this paper is intended for distribution to participants ahead of time so that if any questions arise on it or other topics, they can be sent to me before 30 April 2011 so that I can respond prior to the workshop. In addition, a video keynote address will be presented at the workshop.

SUGGESTIONS: In preparation of background material for the workshop I:

 Used Biology and Conservation of Horseshoe Crabs (2009), The American Horseshoe Crab (2003), and Biology of Horseshoe Crabs (1988) as guides;  Assembled and read recent papers on populations (viz.: papers co-authored by David R. Smith et al.; Winston Watson III et al., etc.);  Assembled and read recent papers on habitat (viz.: Jackson, Nordstrom 2009; Jackson, Smith, Nordstrom 2008; Jackson, Nordstrom, Smith 2002; etc.);  Prepared the attached background information, based primarily on what authors have sent to me (my thanks to them, as I do not frequently get to libraries) and some internet searches. Within the past two decades there probably have been more publications on Limulus polyphemus than in all previous years on a wide range of topics including spawning, fecundity, egg transport, population dynamics, distribution and migrations, fossil species, and habitat changes, etc. So much, it seems to me, that much effort will be needed to assimilate what has accumulated.  Developed a table of questions and answers pertaining to Limulus, as a guide to preparation of what would be more pertinent to the Asian species.

The following material may not be the information that you expected or hoped for. If so, I am willing to attempt to provide it and to answer questions on Limulus, prior to the workshop.

Please send questions to [email protected] before 30 April 2011.

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Limulus polyphemus as a Model for the Conservation of Horseshoe Crabs

Carl N. Shuster Jr. Virginia Institute/School of Marine Science, The College of William & Mary March 2011

PROLOGUE

I am honored and humbled by the invitation to keynote ways in which Limulus might serve as a model for the conservation of Asian horseshoe crabs. This is a challenge because we are in an upward trend of research on Limulus that is related, in part, to conservation and management of the species and there are so many others who are well-aware and involved in Limulus conservation issues. One such expert, the late Dr. Robert B. Barlow, known for his many contributions to understanding vision, circadian rhythms, and spawning in Limulus would probably advise up to look after the “little ones” – meaning, of course, populations of lesser numbers of horseshoe crabs. He would speak emotionally but accurately and succinctly of his experience in having his research population wiped out by commercial harvesting (Weiner and Barlow 1999); (Figure1). Due to his incisive insights and his many contributions on Limulus, I respectfully request that this workshop be dedicated to the memory of Dr. Robert B. Barlow.

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INTRODUCTION

A call for international coordination in the pursuit of the conservation and management of horseshoe crabs was a theme of the symposium held in 2007 at Dowling College, U.S.A. (Tanacredi et al. 2009). It and the report of its panel on horseshoe crab management (Berkson et al. 2009) were direct precursors to this workshop. The panel, comprised of representatives from five countries, responded to eight questions prepared by Berkson. They generally agreed that:

 Basic data necessary for assessment of the status of the horseshoe crab populations had not been collected.  Habitat degradation and loss was the primary threat to the populations.  Primary focus must be on protecting spawning and nursery habitats.  A citizenry educated on the importance of the crabs, especially the policymakers, is essential.  Information and lessons learned during research and management in other countries should be made more directly available through regularly scheduled meetings.  Funding should be sought, especially at the ecosystem-level.  In contrast to the general unanimity on the first seven questions, opinions regarding the future of horseshoe crab conservation ranged from pessimism (Taiwan and China), to cautious optimism (India), to guarded optimism because there was still time to thwart some major threats (Mexico), to outright optimism (USA) due to successful coordination of coastwise management by the Atlantic States Marine Fisheries Commission.

Defining Conservation

Everyone “knows” what conservation is, but do we agree on a definition? As a country boy, trained at a land grant college, it is perhaps natural that I emerged as a believer in conservation as the wise use of a resource. That may not be the concept applicable to the goals of this workshop. In any case, I believe we should define the term. As part of the discussion I would point out that we may not be able to save all populations of horseshoe crabs. If not, is the information obtained and recorded on a population an adjunct to saving it or at least remembering it?

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Scope of the Following Material

Participants of this workshop most likely will be called upon to evaluate available information on the Asian species, determine what else should be obtained, and then decide, at the very least, what actions could be taken to conserve and protect the Asian horseshoe crabs. This paper calls attention to what has been learned about the science, conservation, and management of Limulus populations that may provide a useful background for the development of a conservation strategy for the Indo-Pacific horseshoe crabs. It concentrates on the first two of the four workshop themes (Populations, Habitats, Exploitation/Utilization, and Public Consensus).

Why Look To Limulus?

The suggestion that Limulus polyphemus, the American horseshoe crab, can serve as a model for the conservation of the Indo-Pacific species is based on a large amount of scientific information on the natural history and ecology of Limulus polyphemus, as well as programs to manage its populations. This information and experience provides a sufficient background to begin the discussion on conservation, despite major differences in the natural and political patterns of the distribution of Limulus and that of the Indo-Pacific species.

One glance at the distribution of the Asiatic species is sufficient to appreciate the dedication of Dr. Sekiguchi and his colleagues in the difficult task of mapping and studying such diversely situated populations (Figure 2). Even a casual inspection of the figure suggests that the number of horseshoe crab populations around Borneo is an invitation for an in depth study, particularly due to the presence of all three Asiatic species. There is a long history of research on the Asiatic species, especially Tachypleus tridentatus, exemplified by an excellent treatise on the Biology of Horseshoe Crabs edited by Koichi Sekiguchi (1988). Thus the challenge is to select and utilize what is pertinent from our collective experiences. Much research on Limulus has occurred in recent years; even a summary of that research would create a book. Because I have selected items emphasizing populations and habitats that illustrate or contribute to the conservation theme of this workshop, this selection does not evenly reflect all that is available.

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In contrast, all of the populations L. polyphemus, except the more ancient ones on the Yucatan peninsula, are located within the boundaries of the United States of America and relatively easy to get to. Because the sequence of spawning along the coast is staggered, being slightly later and later as one travels northward, it is possible to observe the spawning of a majority of the populations on the Atlantic coast from Florida to Maine in one summer (Figure 3). In another summer, the Gulf of Mexico population, from Florida to the Mississippi delta, could be examined, including an expedition to Yucatan. These distributions have the distinct advantage of not only that of relative accessibility but also the opportunity to quickly observe many populations along an appreciable environmental gradient, from about 21o to 44o N, during one or two spawning seasons. In a world-wide search Mikkelsen (1988) has also contributed to observations on distribution of the four species.

An important difference between managing/conserving the American and the Asiatic species of horseshoe crabs is that fewer nations and jurisdictions are involved in North America.

POPULATIONS

There are at least two guiding principles when considering the ecology of horseshoe crabs -- they are environmental generalists and they exist in discrete populations. Generally the adaptation of horseshoe crabs to their habitat or environmental factors have been subjects of prime interest (see Towle and Henry 2003). Recently questions have been raised about the genetic viability of populations have been raised (Faurby et al. 2010). Perhaps more closely pertinent topics are considered here: population size; distribution limits including influence of abundance; egg size and spawning events, etc.

Environmental Generalists.

Horseshoe crabs are capable of adapting/adjusting to and surviving manifold variations in their environment (Eldredge 1991, Loveland et al. 1997). They are also rugged, not only in relation to the hydroclimate but also to physical impact due to occasional high energy waves, dredges, and loggerhead turtles that

5 bash/dent or rip away part of their carapace; healing often follows even extensive wounds.

It can be argued that, in addition to their physiological capacity to adjust to estuarine conditions, their survival as a group is due to an architecturally solid, three-part body design with two articulations – a piano-hinge between the first and second parts and a universal joint between the telson and the mid-part. The lineally arranged thirteen, multi-articulated appendages all operate under the carapace, as in a caisson, protected from outside interferences and capable of carrying out, more effectively, such functions as burrowing, spawning, feeding, and locomotion. That they cannot back up appears to be the only major flaw in their mechanical abilities.

Discrete Populations.

Because Limulus polyphemus has morphometrically distinct populations, Shuster (1955) advanced the possibility that the species existed as physiological races. The morphometric discreteness was amply confirmed by Riska (1981). DNA and related analyses clinched the concept and substantiated without a doubt that Limulus existed in genetically discrete populations (Saunders et al. 1970, Selander et al. 1970, Pierce et al. 2000, King et al. 2005).

Thus, although Limulidae have been considered to be “living fossils,” based on their morphology, they have been actually keeping pace, physiologically, with changes in their long-term environment. Ranges in the behavior and physiological characteristics of horseshoe crab species are usually presented in summations based upon many disparate populations. Because this results in a species range of characteristics rather than that of one of its populations, I wonder: Do we really know the extent of these ranges in each of even several populations? Not being sure how many populations there might be, I undertook a quick tabulation of sites where Limulus has been reported. As rough as that review was, it seemed as though Limulus wanders almost everywhere (e.g., Figure 4).

I wonder if it would be worthwhile to survey the U.S. coastline (or any coastline) in detail and determine how many horseshoe crabs populations exist and approximately the total number of these crabs. Actually, because most states have at least surveyed their horseshoe crab populations, with some states actively conserving that resource, it should be relatively easy to prepare an atlas on the

6 abundance and distribution of Limulus polyphemus, including a review of their habitats. Perhaps an atlas could be made of the Indio-Pacific species, starting with the results from the first such survey by Sekiguchi and colleagues (see Sekiguchi 1988).

Does Population Size Matter?

Delaware Bay, touted as the largest population and epicenter of Limulus, is probably not the best source of the answers we seek for the conservation of the Asian species which may be in the populations of lesser numbers category. Dose this require specific definitions? What do we mean by a “larger” or “lesser” population? What are their characteristics? Is one factor the stress level of coping with the hydroclimate (e.g., the salinity, temperature, oxygen mix) of their environment? Is another the restrictions placed on a population due to the size of the environment? Or by the distances that the members of a population travel to compete, in essence, the life history of the population?

In considering these questions and others where, geographically, do we look for populations that might provide the answers? For Limulus, the most northern populations in New England waters are among the “lesser” populations and appear to be pushing the envelope of existence, a least in a cold-water hydroclimate. Those in Maine, especially at Taunton Bay (Moore and Perrin 2007), fit this category. Pleasant Bay, Massachusetts is also semi- to largely restricted in its perambulations (Carmichael et al. 2003, Smith et al. 2009). Other populations are also pushing the envelope of existence as those in a hyper-saline, high-temperature, micro-tidal lagoon at Cape Canaveral, Florida (Ehlinger & Tankersley 2009). We could also consider the populations on the Yucatan Peninsula (Zaldivar-Rae et al. 2009) that was isolated from all other Limulus populations in the distant past; how much is this reflected in their basic biology/ecology? Genetic (King et al. 2005) makeup? Considering the distribution of the Asiatic species (Figure 2), are there any long-term isolations? Are there any particularly interesting populations?

How Many Asian Populations of HSCs? Many of the mainland populations in Asia are no longer as sizeable as in former years. While it is desirable to protect them and to enhance their chances of survival, if for no other reason than to have a national resource that the public can treasure, should all populations, even those in

7 most obscure regions be considered? If the objective is to protect the species then most of the populations of all three species should be considered.

Should mating and spawning behaviors be considered? In this there are a few marked contrasts between Limulus and the three Indo-Pacific species. Yet it seems that the basic spawning unit in all species is single-pair mating – a female will not spawn (at least in Limulus) if a male is not attached (in amplexus) according to Brockmann (2003). The fact that the Asiatic species have two pairs of claspers versus one pair in Limulus seems to be correlated with spawning behavior. The males of Tachypleus tridentatus (Botton et al. 1996) and presumably also the other Indo-Pacific species, secure a more secure lock on the female opisthosomas and the attachment lasts much longer than in Limulus. The weaker attachment in the American species may have led to its alternative behavior of mainly seeking mates on beaches; this results in an abundance of males, with most participating as unattached satellites during spawning.

Spawning Schedule Depends Upon Number of Eggs? A rough calculation indicates that a female Limulus lays 20,000 eggs during a high tide -- about the number of eggs in the major oviducts at the time of spawning (depending upon the age, size, and health of the individual). This, 5 high tides, compares favorably with the two to six spawnings recorded by female crabs tagged with a combined acoustic and radio transmitter and a plastic ID button (Brousseau et al. 2004). Between each spawning the tagged females tended to remain offshore within an average of 299m near the same beach. They usually repeatedly returned to the same beach within an average of 351m from the tagging site, thus creating a seasonal beach-site-spawning-fidelity. Objectively, where else were they going to go? To recap: if a female containing approximately 100,000 mature eggs makes 5 nests a tide with each nest containing about 4,000 eggs, she could completely spawn within five tides. Then what? Presumably these spawned-out females leave the area for deeper water in the bay or on the continental shelf (unless abundant prey is available and the shallow near-shore area). A fair number possibly leave Delaware Bay soon after spawning; at least some do, as observed by Oates (pers. comm., 2005) via use of cameras mounted on a benthic sled. Earlier Shuster and Botton (1985) and Botton and Ropes (1987) recognized the possibility of an offshore migration. This may also be the case for Tachypleus tridentatus (Sekiguchi 1988). Do the other Asian species have a similar spawning “schedule”?

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Would such behavior, of spawned-out females retiring to deeper waters within a bay or on the shelf have any bearing on conservation or management plans?

Botton and Loveland (1989) pointed out, due to the likelihood of stranding, that spawning was a hazardous activity. Areas, where the crabs lack the ability to orient themselves with respect to water when level/flat tidal flats are exposed during low tides, are also hazardous (Botton & Loveland 1987). Considering that the number of times a female horseshoe crab comes to a beach to spawn could increase the chance of her stranding, would the number of trips be correlated with the number of eggs and the time it takes to deposit them?

Despite their Wide Ranges, Horseshoe Crabs Have Limits. Examination of the ranges of the extant species reveals that there are few large-scale limitations to their distribution (Sekiguchi & Shuster 2009, Shuster & Sekiguchi 2009): they are dependent upon low-energy beaches of estuaries; cannot jump an ocean abyss (are limited by the extent of continental shelves); essentially limited to tidal regimes that are diurnal (regular and irregular), and have not been able to attain breeding populations in northern climes beyond 45oN. Locally horseshoe crabs usually exist in discrete populations:

1. Depending upon where they are situated within the range of the species, it seems obvious that most populations would be incapable of immediately surviving in a much more extreme environment. This has been illustrated by a couple of simple temperature trials (Mayer 1914, Fraenkel 1960). They were principally concerned with lethal high temperatures. Cold temperatures are not necessarily lethal as the crabs may survive being frozen in ice at Delaware Bay (according to Thurlow Christian Nelson, Rutgers University, pers. comm. 1947). Limulus begins spawning at a minimum temperature of 12oC in Maine waters, predominately occurring at 14oC (Schaller et al. 2002). Due to the length of time the water is so cold in Maine, this could result in insufficient time to grow (i.e., put on enough weight to trigger the molting process). Born (1977: p.30) believes otherwise. He suggested “… that temperature will not prove to be a primary limiting factor influencing the distribution and breeding success of Limulus at the northern end of its range.” Whatever that threshold may be, Limulus does not maintain populations further north.

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2. Populations at the extreme limits of their geographic range are likely to be under more stress than those within their mid-range.

3. Populations isolated from others are more likely to be genetically more removed.

4. From a physiological viewpoint those populations most under stress or more isolated are most likely to reveal trends or stasis, respectively, in evolution.

5. As a species, horseshoe crabs exhibit wide tolerances to environmental parameters, but members of discrete populations have a lesser range of tolerance.

6. That horseshoe crabs move in the direction of benthic currents is common knowledge (Anderson and Shuster 2003). Michael F. Oates (2007 unpublished) has observed that migrating horseshoe crabs have an unusual sense and use of tidal currents. Observed, with a benthic sled fitted with optical sensors, crabs migrating from Delaware Bay burrow in during a slack tide and then continue on their way when the current flows again in the direction they were travelling.

7. Horseshoe crabs are wanderers as evidenced by several tagging and electronic-sensing programs (Shuster 1950, Baptist et al 1957, Swan 2005, Smith et al. 2005, Watson et al. 2009) and, after the large ice shield that covered North America some 11,000 to 13,000 years ago began to melt (Chrzastowski 1986), by their expansion from southern climes to Maine within a few thousand years. King et al. (2005) believe that female horseshoe crabs return to their natal bays to spawn but the males, being more inclined to wander, are the sex responsible for gene distribution. Yet, a 17-year tagging study reported by Swan (2005) clearly demonstrated that females are also wanderers, some moving 100 km or more from their tagging sites. Nowhere is this better illustrated than the range of crabs entering and leaving Delaware Bay, from Toms Cove to Atlantic City (Figure 5).

Delaware Bay Population is Increasing Again

Horseshoe crabs were still abundant in Delaware Bay during the 1990s (Figure 6), when environmentalists predicted their decline to extinction along with the migratory shorebirds. Some reports are no better today. A recent interpretation of genetic data claims that horseshoe crabs are declining (Faurby et al. 2010). Nor have spawning indices (Smith et al. 2005) indicated a marked increase in

10 spawning. In contrast there is positive information. Whatever the population size might have been during the past couple of decades, adults now number an estimated 20 million (90% confidence interval: 13-28 million) of which 6.25 million were females (90% CI = 4.0-8.8 million); (Smith et al. 2005). That is a substantial number. In 60 years of observing the abundance and distribution of the crabs in the area, I have never seen so many as in the past four years. In recent years on several beaches they have often paved a beach two-tiers deep (Figures 7 and 8). And, upon these tiers, a few females with attached males wander about, even reaching the uppermost edge of the spawners before ultimately retreating back to the bay. Seemingly these females having given up ever finding a spot in which to spawn on that tide.

Abundance and Distribution

Over the years it has been increasingly evident that the distribution of Limulus is, at least in part, due to its abundance. Nowhere is this as evident as the far-ranging crabs of the Delaware Bay area (Shuster 1985, Swan 2005). By comparison, crabs in populations of lesser numbers do not stray very far. At Taunton Bay, Maine (Moore & Perrin 2007) or in four coastal embayments on Cape Cod, Massachusetts (James-Pirri et al. 2005), distances travelled from tagging sites were related to the size of the embayment and its accessibility (the size of its entrance/exit area). The ranges of movement were generally within 2-3 km of the tagging site within the restricted entrance embayments and up to 7 km in the larger ones. These and similar studies provide a key element to our consideration of the conservation of the crabs – that Limulus populations differ among embayments within a region, at least due to environmental conditions and extent of enclosure. Behavioral patterns may also be part of this, as, for example, cannibalism and different migration patterns of the adults – as when the females leave Delaware Bay prior to the males. For the time being, the observation that abundance drives distribution can be considered a working hypothesis.

Another Consideration

Somewhere in the development of conservation plans certain dimensional variables should be considered. For example, what number of individuals

11 comprises a viable population and how large (extensive) must the habitat complex of shoreline, shallow and deep water be? Should this be determined on a case-by- case basis?

Genetic Definition of Populations and Conservation.

The first reports on the discreteness of populations were based on morphology and morphometric analyses (Shuster 1955, Riska 1981). Studies on the genetic component of the evolution of Limulus have been shaping our views on that evolution beginning with Saunders et al. (1986); Figure 9. King et al. (2005) have suggested that there are regional management units of Limulus based upon an apparent substantial gene flow between each population and with its nearest neighbors, mediated perhaps by a male-biased dispersal (i.e., the females do not wander as much). Five regional management units have been defined: Florida-Gulf of Mexico; Florida-Atlantic; Southeast U.S. (South Carolina and Georgia); Mid- Atlantic; and, the Gulf of Maine.

Genetic Diversity and Survival: A Speculation. According to Degener (2010), Tim King, based on a genetic study (Faurby et al., 2010), explained that while the overall population of Limulus has declined since the end of the last ice age, his bigger concern was the “effective population” decrease. The definition of an “effective population” was the number of horseshoe crabs necessary to create the genetic diversity to successfully adapt to changing conditions. Co-author Matthias Obst (Press release 4 Oct. 2010, University of Gothenburg) essentially repeated that conclusion: “We noted a clear drop in the number of horseshoe crabs at the end of the Ice Age, a period characterized by significant global warming” and added “Our results also show that future climate change may further reduce the already vastly diminished population. Normally, horseshoe crabs would have no problem coping with climate change, but the ongoing destruction of their habitats makes them much more sensitive.” If Delaware Bay is an example of what may occur elsewhere, one spawning site may disappear (Figure 10) while another is developing. In a similar setting but in the extensive tidal stream/marsh complex behind Fortesque, New Jersey, there are several new spawning sites that may be expanding (observed by Shuster when accompanying Mr. Michael Oates who was navigating through the numerous tidal stream waterways to observe the habitat situation in 2005).

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Limulus Increased After Last Ice Age

Several ice ages ago, horseshoe crabs may have freely wandered between the Gulf of Mexico and the Atlantic Ocean (Figure 11). This may have been the cause of the genetic makeup of Limulus populations now on either side of the Florida peninsula (Figure 9).

Today, Limulus ranges northward to Maine, with the largest population in the Delaware Bay area. Because this bay did not exist during the last ice age or until a few thousand years later, where were the horseshoe crabs? It seems logical to assume that they moved northward from a southern site, perhaps as far south as Georgia or Florida. Kreamer and Michels (2009) estimated that the spawning of Limulus at Delaware Bay gradually increased over the last 3,000 0r 4,000 years during the time that the bay was evolving (Figure 12). Delaware Bay now supports a population of some 20 million adults (Smith et al. 2005). The size of this population challenges the conclusion (Obst: University of Gothenburg press release 4 Oct. 2010) that there was “…a clear drop in the number of horseshoe crabs at the end of the Ice Age.”

Is Geologic Time A Factor? About 140 million years may be the geologic timeline within which horseshoe crabs have diverged into the four extant species (Figure 14). Limulus diverged from the Indo-Pacific species some 150 to 135 million years ago (mya), followed by a split in the genus Tachypleus between 110 and 20 mya which led to T. gigas and the branch that produced T. tridentatus and Carcinoscorpius rotundicauda some 43 to 8 mya (Sugita 1988, Shishikura & Nakamura 1988). If major ice ages occurred about every 100,000 years during the past one million years (Schirber 2005), global warming probably peaked during the intervals. The result of the interplay between genetic mutations and environmental changes during these episodes of global temperature changes produced the four species that have survived to today. That is the essential point -- four species of horseshoe crabs or their antecedents have survived several global climate changes.

Wrap Up re Populations

Due to my early studies in New England waters, I believe that the studies there may be being more pertinent to conservation issues in Asian than information on the Delaware Bay situation. Unfortunately there are few papers scheduled on

13 the lesser populations in this workshop. However, those authors should be able to support the case for understanding what goes on in the lesser populations. Advance supporting information is readily available in Biology and Conservations of Horseshoe crabs (2009), Chabot and Watson (2010) and in the situation on the Yucatan Peninsula (Zaldivar-Rae et al. 2009) and microtidal lagoons (Ehlinger & Tankersley 2009).

HABITATS

While habitats are not discrete, in the same sense that populations are, a good case can be made that many if not most habitats are unique. Indeed, many of the behaviors exhibited by Limulus can be attributed to the adjustment of the crabs to certain local environmental parameters such as tidal amplitude, benthic currents, prey, and quantity and quality of the habitat.

Broadly considered, geological processes are what determine the extent of habitats favorable to horseshoe crabs. Although these processes are not the topic of this discussion, a series of studies at Delaware Bay should be collated as a handy reference (see papers coauthored by Jackson & Nordstrom 2003, 2009). Assessing and mapping critical horseshoe crab spawning habitats have also been undertaken (Lathrop et al. 2006).

Suffice it to state here that the familiar sequence of erosion – transport - deposition and the encroachment of land into aquatic areas or inundation of land by water undoubtedly would create new habitats as older ones vanish. The general reaction is to deplore the loss of habitat and to try to stop it rather than anticipate creation of new habitats by natural processes or abetted by human endeavor (Titus 2003).

Sekiguchi and Shuster (2009) and Shuster and Sekiguchi (2009) reviewed the information on restrictions to global distribution and local environmental conditions, respectively. The conditions restricting global distribution largely define where horseshoe crabs have and can exist. Adaptation to local conditions illustrates the ecological generalist capability of horseshoe crabs. These environmental and biological conditions are among several factors that invoke a

14 number of questions including anthropological stresses and environmental changes. Speculation on the newest stress is that it will occur due to global warming (Faurby et al. 2010).

On a lesser scale, locally, horseshoe crab eggs are transported by waves and swash, as demonstrated at Delaware Bay (Nordstrom et al. 2006). When wave energy is low the probability increases that eggs will remain on the beach compared with dispersal and burial, with fewer eggs on the surface, during high waves when more eggs are transported in the swash.

Global Constraints on Distribution

There are four major constraints on the distribution of the extant species of horseshoe crabs. Presumably these restrictions were also effective during the times of the fossil species:

1. Horseshoe crabs are unable to cross an oceanic deep. The continental shelf is the pathway for their migrations between bays and land masses. 2. Those shores that provide successful incubation for horseshoe crab eggs are generally bathed by regular or irregular diurnal tides. 3. Horseshoe crabs, at least the three Asian species, tolerate tropical conditions and are found north and south of the equator (Figure 2). However, all the populations are restricted at northern latitudes (Figures 2 and 3). 4. The extent and condition of contiguous estuarine habitats are essential. Beaches provide incubators for the eggs, shallow coastal waters are nursery areas of juveniles), and the deeper waters, often including the continental shelf where large juveniles and adults also feed and hibernate.

Local Environments

Spawning areas are certainly more susceptible, if not the most susceptible, to harm. But not all beaches, mangroves, or intertidal sand flats are equal in value as incubators. Therefore, it would seem that evaluation of sites as incubators should be a prime concern rather counting the number of horseshoe crabs that spawn on them. Just because Limulus spawns in greater numbers on certain beaches does not necessarily identify those beaches as superior incubators. Should we aim to

15 evaluate of a beach in terms of a ratio such as: the number of females versus the number of eggs that develop to maturity?

Each of us has probably witnessed natural and man-caused loss of habitat – a loss that has been assumed to be harmful to horseshoe crabs, as in Figure 15. But it may be that local, short-term changes, such as erosion of some beaches, might not have long-term impacts because new beaches could be forming elsewhere. Anyway, horseshoe crabs are hardy creatures – they are survivors. Over the millions of years that the four extant species have lived, there must have been circumstances where the hardiness and other characteristics of the crabs were important factors in their reaction and survival. Somehow they kept pace in relation to changes in their environment.

Will Horseshoe Crab Habitats Be Destroyed During Climate Warming? Yes but probably not to any great extent, as it is most likely that geologic processes at the edges of the pertinent continents will be similar to those that have occurred before and new suitable habitats will be amenable as habitats for Limulidae. Examples of once fauna-rich aquatic environments that included horseshoe crabs, now at the center of North America (Mason Creek, Shabica and Hays 1997) and Bavaria, Germany (the Solnhofen limestones, Barthel et al. 1990), illustrate the disappearance of species and habitats. But similar habitats develop elsewhere and some species did survive major extinctions, e.g., Paleolimulus avitus.

Limulus habitats have undergone observable changes during the past 50 years. During that time, sea level has been rising almost imperceptibly and most of the natural changes to the spawning beaches, abetted by sea level rise, have been due primaerily to strorm erosion. Over the next several thousand years, sea level rise will be inundating coastal landscapes of different types, ranging from coastal plains to piedmont (Figure 13). This recalls a saying by the “old timers” of Delaware: “There is only one county at high tide;” the other two, more southerly are as flat as a pancake. There may be times when large areas are no longer habitable by horseshoe crab. However, there is no reason to assume that geologic processes in the future will markedly differ from current ones, so new habitats suitable for horseshoe crab spawning probably will be created. Under these conditions, a warming climate does not appear to be a serious factor in the survival of horseshoe crabs. The Asian species already exist in tropical climes. Warmer

16 waters to the north would seem to offer an extenstion of the present range of Limulus into Canadian waters where outliers have been occasionally reported.

There is also the possibility that the relative confinement of horseshoe crabs within a limited access/egress habitat might make them more prone to genetic stasis or to an abrupt change in a local condition such as a food source (e.g., when a major food source – blue mussels – is threatened by increasing commercial dredge harvests). The fate of such populations, it seems to me, is less fortunate than for those with a wide-open access to a larger habitat via a larger body of water. But since all of this may play out over a geologic time scale, does it really matter? Or should we concentrate on populations in the more favorable habitats?

Impact of Global Change: Speculation

Several news releases that followed the publication of Faurby et al. (2010) have speculated that global warming is one of the causes of declines in populations of Limulus polyphemus. By implication global warming should have impacted each of the extant species during their length geologic history. Sea-level rise is certainly associated with global warming and, if Delaware Bay is an example, beach quality and quality have been demonstrably diminished, especially by erosion due to storms (Figure 15). However, there are ample irregularities in the elevation of land such that encroachment of rising seas would also be irregular. Further, the tolerance and adaptability of horseshoe crabs to a wide range of temperature (Mayer 1914, Fraenkel 1960, Reynolds and Casterlin 1979) suggest that they should be sufficient to survive any water temperature fluctuations due to global warming. It would seem that the speculation about losses of beaches and temperature fluctuations in the hydroclimate is overdone when examined within the context of geomorphic changes in the coastline and the hydroclimate during the millions of years that the four extant species has existed, This probably was a certainty for Limulus after the last great ice ace (13,000 – 11,000 years ago), at least along the Atlantic coast of North America. The distribution of the Asian crabs throughout the equatorial area suggests that warm temperatures are not all that limiting. Apparently no studies have addressed the question of long-term exposure to higher temperatures, especially in relation to ovulation and fecundity.

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Also, prior interpretations, as expressed by Avise (2002), held that the extant horseshoe crabs “…are exceptional in levels and patterns of genetic variability, both within and across species. On other words, most of their genes give no indication of “aberrant” evolutionary generic rates or processes compared with other kinds of animals.” Avise also observed that the body plan that evolved so long ago apparently worked so well that it was retained “Yet, internally, their molecular genetic clocks have kept on ticking.” He also cautions “…don’t underestimate these resilient beasts...” they “…have witnessed mountain ranges rise from the sea and continents drift across the full face of the planet.”

Visualizing Environmental Variables

Independent variables such as water temperature and salinity can be combined in a climatograph as an aid in the visualizing spatial and temporal differences of these variables in the same or several other habitats. The graphic method adopted from terrestrial studies by Hedgpeth (1957) has been used here to compare the water environments (salinity and temperature) of Great Bay, New Hampshire, and Delaware Bay (Figure 16). Variations between these two environmental factors can be due to differences in the evaporation and precipitation as well as to the relative amounts of freshwater and sea water in the bays and to their temperatures. During the spring rains, flows from the rivers and streams are generally high and the air temperature has a greater effect upon the river water than the colder seawater; thus river flow may affect both temperature and salinity. The opposite effect may occur during the autumn rains when the river water. Influenced by air temperatures, has cooled more rapidly than the larger body of coastal water.

EXPLOITATION versus UTILIZATION

The term “exploitation,” as contrasted to the overall objectives of “conservation,” seems a too radical characterization of the uses of horseshoe crab resources. A more representative term may be “utilization,” in the sense that conservation is the wise use of resources.

Multiple uses of Limulus polyphemus are well-known (Berkson and Shuster 1999; Walls et al. 2002), including the extensive use of the species in scientific

18 research. Because each use has a different impact upon the crabs and their ecological associates, it may be necessary to consider different conservation measures in relation to different uses. The extremes are obvious – complete protection for ecological reasons (e.g., to protect the crabs and dependent species such as loggerhead turtles and migratory shorebirds) versus unlimited use. In between uses involve those such as the number of crabs used and the relatively low mortality of the crabs bled for LAL production versus their ultimate death as bait.

Managing for Conservation. The conservation objective, whether to preserve or protect a local crab population, protect an endangered species, or manage the species to benefit other species, etc., may require different methods but, in most cases, overall habitat conditions, protection of spawning crabs, and impacts (including harvesting) on a population will probably be the focal situations in need of the greater consideration.

Controlled handling procedures of horseshoe crabs in the production of Limulus amebocyte lysate (LAL) – harvest method, transport, bleeding, and return to the sea – are necessary to reduce external stressors that produce mortalities (e.g., lengthy air exposure, elevated temperatures, etc.); Hurton and Berkson (2006).

After the introduction of bait bags using parts of horseshoe crabs by a Frank “Thumper” Eicherly IV. a waterman whose home pot is Bowers, Delaware, Robert Fisher, researcher in the Virginia Institute of Marine Science - VA Sea Grant Program, determined that one-half a crab, male or female, versus the use of a whole crab, showed a slight decrease in total catch of whelk but the decrease was not statistically different (Fisher 2000). However, further decrease in bait portions, to one-third or one-fourth a crab, sharply reduced the catch.

By far the greatest stimulus for the management and conservation of Limulus arose in recent decades due to a perceived impact on migratory shorebirds by the harvest of horseshoe crabs mainly to bait whelk traps in the mid-Atlantic bight centered on Delaware Bay. All Atlantic states of the United States, Florida to Maine, through the Atlantic States Marine Fisheries Commission (ASMFC 2010), have participated in the management of the total horseshoe crab resource and of local discrete populations since 1999; the Gulf Coast Marine Fisheries Commission has been less involved to the present time. The ASMFC management

19 has involved spatial, temporal, and biologically-based restrictions on harvests and the establishment of horseshoe crab reserves.

Management of horseshoe crabs in the Delaware Bay area, where the emphasis is upon the availability of the crab eggs for migratory shore birds that stop in the area to refuel on flights from the south on the way to northern Canada to breed, directly involves the fisheries in the states of Delaware, New Jersey, Maryland, and Virginia. Thus, in this case, the most sensible and direct way to manage egg production is to protect the adult females. This can be accomplished by banning harvest of all crabs or banning harvest of the females and limiting the taking of adult males. In recent years New Jersey has banned all harvest while Delaware has limited the harvest to 100,000 males per year and only after the spawning season. Banning harvesting during the spawning season has two benefits: lessening impacts on the breeding crabs and on the sensitive migratory shore birds. The harvest of Limulus males is viable due to the special spawning behavior in which the males tend to remain in the near-shore region and repeatedly come ashore to mate throughout the season, often creating ratios of 3 to 5 males per female on the beaches. This harvest of a portion of the skewed sex ratio favoring Limulus males on the beaches would not be possible in the Indo-Pacific species where single-pair mating (one female with her amplexed male) is the dominate mating behavior. However, the essential management strategy, for either type of mating behavior, is to protect the animals during their spawning years, particularly the females (Figure 17), and their spawning sites.

Sometime during the development of conservation plans, consideration should be given to the consideration of certain dimensional variables. For example: what number of individuals comprise a viable population, and how large (extensive) must the habitat complex of shoreline, shallow and deep water be? A recent series of studies (e.g., Smith et al. 2009 and others with Smith) should be collated as a compendium on methods of studying populations and the kinds of results that can be obtained.

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PUBLIC CONSENSUS

If the term “consensus” is being used to imply the opinion of the majority, this probably can be reached on broad issues but narrow issues may have to be resolved locally. Public consensus should be based, among other factors, upon awareness of the value (i.e., the range of uses of horseshoe crabs) and the health of the horseshoe crabs (Mattei 2008).

Scientists have not reached a consensus on whether the relative numbers of young adults versus middle aged and old specimens can be used as an index on the “health” of a population. The biggest obstacle to identifying the relative age is due to the level of impact of the abrasive environment of the crabs. Because their uneven distribution ensures differences in environments, their carapaces “age” and collect epibionts differently. However, there is no mistaking a first-year adult. It has a shiny carapace that is abundantly “feathered” on the adjacent margins of the prosoma and opisthosoma, is virtually non-scarred (bear no black scratches or wear areas), has no or few epibionts, and is more aggressive than older crabs (feisty, “fighting” when handled); Figure 18.

Several books on Limulus written to appeal to a youthful audience and some of these are quite suitable to introduce adult readers to horseshoe crabs. These appear to have had wide dissemination. Similar books are probably also available on the Asian species; if not, this could be one way of reaching a youthful audience.

Horseshoe crabs have long been revered in some Asian countries as national icons. In comparison, only recently, 2002, has a state in the U.S.A., designated Limulus polyphemus as the State marine animal.

CONCERNING CONCEPTS

I have used concepts occasionally to emphasize a point. Concepts and definitions are the cornerstones of the framework on which I place information on horseshoe crabs. Of these the “environmental generalist” concept is prime, the one on which all information must assessed. The concept of “discrete populations” has been repeatedly been supported by morphological and genetic data and is well- accepted. Whereas, “spawning beach fidelity” is ephemeral rarely lasting more

21 than a season. If we accept seasonal “fidelity” as absolute, then it could be argued that Delaware Bay supports several populations, which it probably does anyway, during the spawning season. Another point of guidance – horseshoe crabs are not fish. They are one of the oldest surviving lines of arthropods and should not be hemmed in, exclusively, even by what we think of other evolutionary lines except, perhaps, the trilobites. That horseshoe crabs are “wanderers” was discussed earlier. And the crabs are significantly guided by benthic currents (Barthel 1974).

EPILOGUE

An Appendix is offered, not as a summary of this paper, but as one way in which information might be organized to aid consideration of the conservation of the Indo-Pacific species of horseshoe crabs. The anticipation is that this appendix and the preceding the text will be circulated to all registered participants well in advance of the workshop. Participants can determine if these two, text and appendix, are pertinent to local and national problems concerning horseshoe crabs and scope out their answers and questions so that, at the workshop, they can hit the ground running -- utilizing what is pertinent about Limulus in the conservation of the Indo-Pacific species. I except all participants will have a working knowledge of the information in Tanacredi et al. (2009); from this book I would concentrate on the recent studies by Smith et al. (2009), Jackson and Nordstrom (2009), and Watson et al. (2009), the references that they cite, and my citations of “lesser” populations in my paper.

A Last Minute Addition. Just as I was finishing up this paper I chanced upon a Current Zoology website: http://www.actazool.org/issuedetail.asp?volume=56&number=5&issue_id+503

Twelve papers in this volume, co-edited by Christopher C. Chabot and Winston H. Watson III, addressed the theme of “Horseshoe crab behavior: Patterns and processes.” The papers dealt mainly with horseshoe crabs in relatively small estuaries where their migrations are somewhat limited. I was also favorably impressed by the paper by a new-comer, Wan-Jean Lee, who used a camera “on a

22 clothes line” to study and photograph, unmolestingly, intensive scavenging on an intertidal flat of Great Bay, New Hampshire, by adult crabs.

This special issue was dedicated in a personal, heartfelt tribute to the late Dr. Robert B. Barlow who was an inspiration to many. Much of his enthusiasm showed in the intensity in which he probed for an understanding of the animal and from his deep interest in and concern for Limulus.

What To Do Now?

In getting ready for the workshop, the preceding discussion and questions -- besides those that may be or are more pertinent to the Asian species – should be answered or identified. This bit of homework was the reason I requested that my written article be circulated prior to the workshop. Meanwhile, Michael “Mike” F. Oates, a documentarian, is making a video with me that will be presented at the workshop.

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Jackson N.L., Nordstrom K.F. (2009) Strategies to conserve and enhance sandy barrier habitat for horseshoe crabs (Limulus polyphemus) on developed shorelines in Delaware Bay, United States. In: Tanacredi J.T., Botton M.L., Smith D.R. (eds.) Biology and Conservation of Horseshoe Crabs. Springer Science: 399-416.

James-Pirri M.J., Tuxbury K., Marino S., Koch S. (2005) Spawning densities, egg densities, size structure, and movement patterns of Spawning horseshoe crabs, Limulus polyphemus, within four coastal embayments on Cape Cod, Massachusetts. Estuaries 28(2): 296- 313.

King T.L., Eackles M.S., Spidle A.P. and Brockmann H.P. (2005) Regional differentiation and sex-based dispersal among populations of the horseshoe crab Limulus polyphemus. Trans. Amer. Fisheries Soc. 134: 441.

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Pre-meeting background material for the 2011 International Workshop on the Science and Conservation of Asian Horseshoe Crabs (13-16 June 2011, Hong Kong, China]

Limulus polyphemus as a Model for the Conservation of Horseshoe Crabs

Carl N. Shuster Jr.1

Virginia Institute of Marine Science, The College of William and Mary

March2011

FIGURES

1 Home Address: 3733 North 25th Street, Arlington, Virginia, USA 22207-5011

[email protected]

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2

Fig. 1. Maximum number of Limulus counted in three 10-m2 quadrats during the 1984, 1990, and 1900 spawning seasons in Mashnee Dike (from Widener & Barlow 1999). The height of each bar gives the maximum number of males and females in a single half-hourly survey each day. The open and closed circles indicate the times of the new and full moons. Surveys were not done on 28 and 30 May 1990 because of bad weather. Data were interpolated for these two days to calculate spawning activity. Periods of observations were 14 May to 8 July 1984; 19 May to 22 June 1990, and 24 May to 16 June 1999.

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Fig. 2. The continental shelf (cs) is the avenue of migration/contact between the three Asian species of horseshoe crabs (based on Sekiguchi 1988). One species or more was found near most of the research sites (small arrows); yellow circles = Tachypleus gigas; green circles = Carcinoscorpius rotundicauda; and, red circles = Tachypleus tridentatus. JA = Japan; CH = China; IN = India, and A = Australia. The south-north axis of the distribution of Tt is similar to Limulus polyphemus, the American horseshoe crab. Could this be a basis for more ecological, similarities between Tt and Lp than those between Lp and Tg or Cr?

Fig. 3. Distribution of Limulus polyphemus; coastal areas in Yucatan (YN) and the United States, between the two sets of arrows, support Lp populations. Sixteen of these were examined by Shuster (1955, 1979): two from Florida in the Gulf of Mexico and the rest from South Carolina to Maine on the Atlantic coast, USA.

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Fig. 4. Wherever the distribution of horseshoe crabs is examined in detail, the crabs seem to be everywhere. The red dots indicate recapture of sonar-tagged crabs on the shores of Connecticut, Staten Island, Long Island, and Narragansett Bay, Rhode Island (from Mattei 2008).

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Fig. 5. Estimated distribution of three populations of horseshoe crabs in the Middle Atlantic Bight: Upper Chesapeake Bay; Lower Chesapeake Bay and the continental shelf off the bay entrance; and Delaware Bay and the adjoining shelf area (from Shuster 1985). The fewer numbers throughout Chesapeake Bay is largely due to the lack of extensive sandy beaches (tidal marshes form much of the undeveloped shoreline). The upper Chesapeake Bay has supported a relatively small population, at least since 1953 (Shuster 1955, 1979). Horseshoe crab spawning sites exist within most embayments along the Atlantic shore of the DelMarVa Peninsula; the largest is at Toms Cove, Chincoteague, Virginia.

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Fig. 6. Slaughter Beach, Delaware in 1999 (photograph by Shuster). The crabs are bunched up near the foot of the beach during an ebbing tide. The stranded crabs mark the upper limits of earlier spawning. This was during the time when the media were beginning to report that the crabs were headed for extinction along with migratory shorebirds that fed on Limulus eggs, especially the Red Knot. Management of Limulus harvests at the state level began in the 1990s in the Mid-Atlantic States (Shuster 2003).

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Fig. 7. A moderately heavy Delaware Bay spawning at Mispillion Harbor at 1548 hrs on 19 May 2006 (courtesy of Greg Breese, Delaware Bay Estuary Project, U.S. Fish & Wildlife Service). Nest depressions in the upper right corner of the scene and the positions of several of the spawners, especially in the lower right corner, suggest this was during an ebbing of the tide. This illustration was used in several news items during October 2010 that warned of a negative impact on horseshoe crabs by global warming. Such a large number of spawners, as seen in this sample, does not fit that speculation. Especially since such numbers were also seen on other beaches. According to observers of spawning in the early 1990s, the author included, the number of spawners then and in this scene were comparable -- it was during the in-between-years that the horseshoe crab population was possibly only 40% to 60% as great. Whether conservation measures such as male-only harvests, an embargo on the taking of adult female crabs, and the establishment of a large sanctuary off Delaware Bay (Figure XX) were mainly responsible for the resurgence of the population can be argued, but it certainly is increasing!

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Fig. 8. Limulus spawning on Pickering Beach, Delaware on Delaware Bay, on the new moon in May 2010. This was a heavy spawning with the band of spawners extending at least four meters from the uppermost spawners on the beach to the disappearance of the band into the bay; these numbers also extended at least 100 m along this beach. There is only one old male in this view (the one with the blackened carapace on the extreme right) and a mid-aged male (half-off the bottom of the picture). The rest of the crabs, mostly males, as the females are beneath them, are first-year spawners (the ones with the lighter-colored, shiny shells) and second- and third- year spawners (slightly older ones with black scratch marks and discolored rims); courtesy of Glenn Gauvry, Ecological Research.

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Fig. 9. The 15 populations examined by Saunders et al. (1986): Florida – Panama City, Panacea, Tampa Bay, Ft. Myers, Islamorada Key, Stuart, Cape Canaveral; Georgia – three sires including Sapelo Island; North Carolina -- Beaufort; New York – Long Island; Massachusetts – two sites including Pleasant Bay; and, New Hampshire – Dover Point. There were two major mtDNA clonal assemblages: horseshoe crabs in Florida waters versus those from Georgia to New Hampshire.

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Fig. 10. This panorama was taken in the summer of 1979 near the old exit of the Broadkill River into Delaware Bay (formerly at the south end of Broadkill Beach, near the left foreground in this view but completely closed by 1979). Small numbers of Limulus were still spawning in this area in the 1970’s. The river entrance closured finally after several decades of openings and temporary closures associated with storms.

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Fig. 11. One million to 700,000 years ago (mya) a balmy tropical environment, the Aftonia Interglacial Stage, existed in a southern Florida (Petuch 1992). A large inland marine sea, the Okeechobean Sea, was fringed by coral reefs. Mollusks, chiefly gastropods, were abundant; oysters and scallops were also abundant. Two major channels (straits) connected the sea with oceanic water to the west and east; strong currents passed through these channels during tidal changes. No fossil horseshoe crabs have been found there but they almost certainly inhabited this sea.

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Fig. 12. Three stages in the formation of present-day Delaware Bay (from Chrzastowski 1986): left to right – 15 to 13 thousand years ago when the entrance to the ultimate Delaware River was at the edge of the continental shelf; 11 thousand years ago when the ancestral bay was flanked by capes; 8 thousand years ago when mean sea level (MSL) was still -20 m below that of today. The present land area is shown by diagonal lines; black areas along the margins of the land indicate previous tide marshes. These modifications of the coast illustrate that the shoreline is ever-changing.

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Fig 13. Changes in the mid-Atlantic coastline between ice ages, showing comparisons of the present coastline to estimated changes from the entrance to Chesapeake Bay to Long Island Sound, 12,000 years before the present to 75,000 years in the future (courtesy of John C. Kraft, University of Delaware, 1999).

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Fig. 14. Two estimates of the geological ages of the extant species of Limulidae. Phylogenetic relationships based on:

(Top) the results of micro-complement fixation measurements; it is assumed that American and Asian species diverged 135 million years ago (Shishikura et al. 1982, from Sugita 1988). (Bottom) the “Mutation distance” among peptide “C” of the four species (from Shishikura and Nakamura 1988).

[NOTE: Mesolimulus walchi lived during the Upper Jurassic some 150 million years ago (Barthel et al. 1990; Eldredge 1991); specimens, mainly juveniles are preserved in Solnhofen limestone, Bavaria, Germany. Also see the distribution pattern of extinct and extant species during the Mesozoic and Cenozoic by Sekiguchi (1988, pages 410-414).

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Fig. 15. A “blowout” of a sandy beach exposed an underlying peat bank north of Fowlers Beach in an uninhabited area, Delaware. This type of erosion has occurred several times, turning freshwater impoundments behind the beach that had been created as waterfowl refuges, into saline environments. It is also evidence of the invasion of the shoreline by marshland that was subsequently covered with sediments that were being transported seaward (photo by John Chirea, pilot, of Prime Hook, Delaware in 2007; courtesy of Glenn Gauvry, ERDG). A 2010 U.S. Fish & Wildlife Draft Environmental Assessment describes a program to restore the dune system to minimize impacts of coastal flooding.

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Fig. 16. A salinity/temperature hydroclimagraph for Great Bay, New Hampshire (based Watson et al. 2009) compared with one on the Bar Grounds (oyster beds) in a mid-bay section of Delaware Bay (Shuster 1960).

This graph shows the marked contrast between the affect of freshwater inflow in the estuary (Great Bay) and on the coast in April and May despite the dominance of seawater the rest of the year.

Delaware Bay: A = a graph of average monthly conditions for a 5-year period (1955-1959); B and C are contrasting years - -1955 (a dry summer). -- 1956 (when rainfall from hurricane “Diane” caused a rapid increase of 3.5 times the river flow within 2 days).

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Fig. 17. A horseshoe crab reserve was established off the entrance to Delaware Bay by NOAA, National Marine Fisheries Service in 2001 to protect the heart of the Delaware Bay spawning population, the female Limulus component; the large juveniles that molt in late fall and could potentially spawning the following year and the young adults (2-4-year-olds).

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Fig. 18. A young adult female Limulus presumed to be in her second year of adulthood. The carapace of this female is slightly dulled, in comparison to the lustrous appearance of the carapace of a newly molted animal, but the carapace still clearly shows the fine mosaic detail of the ridges (clear) and valleys (black lines). The angle at which light shone on the opisthosoma highlighted the swales between the fused segments of the Carboniferous ancestor. Also there is a small mating scar on the opisthosoma.

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APPENDIX -- A tabular summary of potential conservation-pertinent information about horseshoe crabs, using Limulus polyphemus as an example.

POPULATIONS

Questions Answers & Questions Problems re Asian spp.? Asian Actions? 1. Do mated pairs or single A one year ephemeral Single pair mating could Inhibit the taking of adults of the Asian species fidelity of Lp is not restrict management; e.g., mated pairs; harvest only always return to their natal commonly repeated, year if only males are collected non-amplexed females; beaches to spawn in to year. Usually local (as with Lp), mated pairs designate some spawning subsequent years? circumstances mediate this would be unconnected. beaches sanctuaries. Any differences in - as along-shore currents, harvesting? & abundance of spawners. 2. Are the wanderings of the Lp sexes appear to move Do Asian spp. Have similar Conduct research if it is sexes significantly independently; females go behavioral patterns? Does deemed essential to different? seaward before the males. it really matter? under-stand crab behavior. 3. How many populations of Not known for Lp, but Will the multi-nation Conduct research to rank a species are necessary for after the last ice age distribution require special the level of criticality for its survival? probably at least double cooperation and each population? the number of populations coordination? occurred. 4. How long does it take a Lp females probably could Could stranding be less; Essential to female to complete an at an average of four high e.g., Tt seems to mainly understanding population annual spawning? Is risk of tides. For Lp risk of spawn underwater? dynamics? If so, conduct stranding increased? stranding is 10%. research.

48 5. Is fecundity a factor? All Lp has the smallest–sized Fewer eggs, larger-sized Conduct research if extant spp. egg numbers & eggs and produces many eggs a survival advantage deemed important. sizes differ. more that the Asian spp. for the early instars? 6. What number of crabs is Recent genetic studies say Most populations have not Determine genetic status needed to maintain a viable populations may be static been studied. of, at least, populations in population? or in a bottleneck status consideration for regardless of numbers. conservation. 7. What is an “effective Considering the survival ? ? population?” What can be of the 4 extant species for done to help an effective millions of years? population evolve? 8. Is it necessary to consider Considering the survival Possibly too esoteric to Consider anyway? the concept of effective of the 4 extant species for reasonably consider. populations as important in millions of years? their conservation? 9. Even if an effective It would certainly appear Examine whether this Develop clear guidelines population could be a to be. The major problem could be used on some if this concept has merit conservation measure, is lack of a reliable ID for populations to advance and is applicable. would a healthy population “healthy.” their conservation. be a satisfactory intermediate goal? 10. If the genetic change It probably is not just the It posits and interesting if A “back burner” issue? posited by Faurby et al. last ice age but other local speculative problem. (2010) occurred within and global factors. some 12,000 years after the last ice age, what occurred during several previous ice ages?

49 11. Is a population the most Yes. Probably the most practical Use. manageable unit of a approach. species for conservation? 12. To what extent is it Certainly those Identify, also, the reasons Proceed as necessary. desirable or even possible to populations most at risk for the risks and what can identify all populations? can be identified. be done to reduce them. 13. Should all populations Depending upon the How discrete are Consider? be conserved, a majority, or circumstances, one of the populations of the Asian selected ones? options should be viable. spp? 14. Because the separate The time line for species What occurs within Consider? evolution of the extant appears to be millions of millions of years is more of species began some 135 years; see Figure 14 in academic interest than of million years ago, is it text. practical use. What possible that a period of The time line for an actuates an “effective” time less than 12,000 years “effective” population population? Would this would produce an effective would be less? concept be helpful in population? conservation considerations?

50 HABITAT

Questions Answers & Questions Problems re Asian spp.? Asian Actions? 1. Are global constraints of This appears to be an Sea level rise, in geologic Determine if sea level rise any importance? academic question, not one time, would probably will markedly affect of every-day importance. change access routes horseshoe crab between populations. conservation planning. If so, how and how soon? 2. Do speculations on the Certainly sea level rise will Patching up local short- Consider combining impact of global warming occur. In long-term term impacts is done horseshoe crab and human have any place in considerations it may not mostly to protect human projects in conservation considerations about matter. Locally and in the activities and projects. planning. conservation? “now” situations it would. 3. Should habitat It has been successful in This is probably a case-by- Consider. restoration/preservation be the USA in conjunction case kind of decision. a part of horseshoe crab with beach fill to protect conservation? buildings and dunes.

UTILIZATION

Questions Answers Problems re Asian spp.? Asian Actions? 1. Should conservation Probably not. A lot would HSCs used in USA (for As required. measures be developed for depend upon the signifi- fertilizers, bait, LAL, each use of HSCs? cance of the use and how watching birds feed on much it would advance the HSC eggs, feed live stock conservation effort. & poultry, etc.); human food in some countries.

51 PUBLIC CONCENSUS

Questions Answers & Questions Problems re Asian spp.? Asian Actions? 1. Will public concerns Is public awareness a Would any survey be of Take appropriate action. and awareness be problem? What would be any value? Or would it be surveyed to arrive at a involved? Spot-checking or better to immediately public consensus? a census? proceed with education? 2. If so, what topics will Uses of HSCs? Any other Results needed at local, Publish results in some be surveyed? values? state, or national level? form? 3. Will it include what And steps to include Will meetings occur among Involve key people at all steps to take to achieve politicians and government local officials (government, levels and in all kinds of conservation of HSCs? fisheries officials? fisheries, and education) activities. with visiting scientists? 4. Will special workshops This has been successful in In 1996 I spoke about Lp to As necessary. or classes be held to several states in the USA. a public school science educate teachers and class in Japan; education pupils? seems to be a universal goal.

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