Endangered and Threatened Wildlife and Plants; Proposed Listing Determinations for Ten Species of Giant Clams Under the Endangered Species Act

Federal RegisterJul 25, 2024

Ask Donna

What actually matters in this document.

Text

DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

50 CFR Parts 223 and 224

[Docket No. 240626-0177; RTID 0648-XF174]

Endangered and Threatened Wildlife and Plants; Proposed Listing Determinations for Ten Species of Giant Clams Under the Endangered Species Act

AGENCY:

National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA), Commerce.

ACTION:

Proposed rule; availability of status review; request for comments.

SUMMARY:

We, NMFS, have completed a comprehensive status review of seven species of giant clams (

Hippopus hippopus, H. porcellanus, Tridacna derasa, T. gigas, T. mbalavuana, T. squamosa,

and

T. squamosina

) in response to a petition to list these species as threatened or endangered under the Endangered Species Act (ESA). Based on the best scientific and commercial data available, including the Status Review Report, and after taking into account efforts being made to protect these species, we have determined that

H. porcellanus, T. mbalavuana,

and

T. squamosina

are in danger of extinction throughout the entirety of their respective ranges,

T. derasa

and

T. gigas

are in danger of extinction in a significant portion of their respective ranges, and

H. hippopus

is likely to become an endangered species within the foreseeable future throughout a significant portion of its range. Therefore, we propose to list

H. porcellanus, T. mbalavuana, T. squamosina, T. derasa,

and

T. gigas

as endangered species and

H. hippopus

as a threatened species under the ESA. We have determined that the fluted clam,

T. squamosa,

is not currently in danger of extinction throughout all or a significant portion of its range and is not likely to become so within the foreseeable future. Therefore, we find that

T. squamosa

does not meet the definition of a threatened or an endangered species under section 4(a) of the ESA. Further, we propose to exercise the discretionary authority of section 4(d) to extend the prohibitions of section 9 of the ESA to the proposed threatened species,

H. hippopus.

At this time, we do not propose to designate critical habitat for the three species proposed to be listed that occur within U.S. jurisdiction (

H. hippopus, T. derasa,

and

T. gigas

) because critical habitat for these species is not yet determinable. Using the authority of section 4(e) of the ESA, we also propose to list

T. crocea, T. maxima, T. noae,

and

T. squamosa

as threatened species due to the similarity of appearance of products derived from these species (

e.g.,

meat, worked shell products, and pearls) to those derived from the six aforementioned species proposed to be listed based on their extinction risk. We propose a special rule to define activities that would and would not be prohibited with respect to these four species in order to mitigate the substantial enforcement challenge associated with this similarity of appearance concern. We solicit information to inform the final listing determination and to inform a future proposal for any determinable critical habitat.

DATES:

Comments must be received by October 23, 2024.

Public informational meetings and public hearings:

In-person and virtual public hearings on this proposed rule will be held during the public comment period at dates, times, and locations to be announced in a forthcoming

Federal Register

notice.

ADDRESSES:

You may submit data, information, or written comments on this document, identified by NOAA-NMFS-2017-0029, by either of the following methods:

•

Electronic Submissions:

Submit all electronic public comments via the Federal e-Rulemaking Portal. Go to

https://www.regulations.gov

and enter

NOAA-NMFS-2017-0029

in the Search box. Click on the “Comment” icon, complete the required fields, and enter or attach your comments.

•

Mail:

Submit written comments to Endangered Species Division, Office of Protected Resources (F/PR3), National Marine Fisheries Service, 1315 East West Highway, Silver Spring, MD 20910, USA, Attn: Giant Clams Species Listing Proposed Rule.

Instructions:

Comments sent by any other method, to any other address or individual, or received after the end of the comment period, may not be considered by NMFS. All comments received are a part of the public record and will generally be posted for public viewing on

https://www.regulations.gov

without change. All personally identifying information (

e.g.,

name, address,

etc.

), confidential business information, or otherwise sensitive information submitted voluntarily by the sender will be publicly accessible. NMFS will accept anonymous comments (enter “N/A” in the required fields if you wish to remain anonymous).

The Status Review Report associated with this determination, its references, and the petition can be accessed electronically at:

https://www.fisheries.noaa.gov/action/proposed-rule-10-species-giant-clams-under-endangered-species-act.

The peer review plan, associated charge statement, and peer review report can be accessed electronically at:

https://www.noaa.gov/information-technology/status-review-report-of-7-giant-clam-species-petitioned-under-us-endangered-species-act-hippopus.

The draft Environmental Assessment and Initial Regulatory Flexibility Analysis associated with the proposed ESA section 4(d) regulation for

T. crocea, T. maxima, T. noae,

and

T. squamosa

can be accessed electronically via the Federal e-Rulemaking Portal by navigating to

https://www.regulations.gov

and entering

NOAA-NMFS-2017-0029

in the Search box.

FOR FURTHER INFORMATION CONTACT:

John Rippe, NMFS Office of Protected Resources, (301) 427-8467,

john.rippe@noaa.gov.

SUPPLEMENTARY INFORMATION:

Background

On August 7, 2016, we received a petition from Dwayne Meadows to list 10 species of giant clams (Cardiidae: Tridacninae) as threatened or endangered under the ESA throughout their respective ranges. The petitioner also requested that critical habitat be designated in waters subject to U.S. jurisdiction concurrently with listing under the ESA. On June 26, 2017, we published a 90-day finding (82 FR 28946) announcing that the petition presented substantial scientific or commercial information indicating that the petitioned action may be warranted for 7 of the 10 species listed in the petition:

Hippopus hippopus

(horse's hoof, bear paw, or strawberry clam),

Hippopus porcellanus

(porcelain or China clam),

Tridacna derasa

(smooth giant clam),

Tridacna gigas

(true giant clam),

Tridacna mbalavuana

(syn.

T. tevoroa;

devil or tevoro clam),

Tridacna squamosa

(fluted or scaly clam), and

Tridacna squamosina

(syn.

T. costata;

Red Sea giant clam), but that the petition did not present substantial scientific or commercial information indicating that the petitioned action may be warranted for the other 3 species (

T. crocea, T. maxima,

T. noae

). We also announced the initiation of a status review of the seven aforementioned giant clam species, as required by

section 4(b)(3)(A) of the ESA, and requested information to inform the agency's decision on whether these species warrant listing as endangered or threatened under the ESA. We received information from the public in response to the 90-day finding and incorporated the information into both the Status Review Report (Rippe

et al.,

2023) and this proposed rule. This information complemented our thorough review of the best available scientific and commercial data for these species (see

Status Review

below).

Listing Determinations Under the Endangered Species Act

We are responsible for determining whether species are threatened or endangered under the ESA (16 U.S.C. 1531

et seq.

). To be considered for listing under the ESA, a group of organisms must constitute a “species,” which is defined in section 3 of the ESA to include any subspecies of fish or wildlife or plants, and any distinct population segment (DPS) of any species of vertebrate fish or wildlife which interbreeds when mature (16 U.S.C. 1532(16)). On February 7, 1996, NMFS and the U.S. Fish and Wildlife Service (USFWS; together, the Services) adopted a policy describing what constitutes a DPS of a taxonomic species (“DPS Policy,” 61 FR 4722). The joint DPS Policy identifies two elements that must be considered when identifying a DPS: (1) The discreteness of the population segment in relation to the remainder of the taxon to which it belongs; and (2) the significance of the population segment to the remainder of the taxon to which it belongs. Because giant clams are invertebrates they cannot be listed as DPSs, and the DPS Policy does not apply here.

Section 3 of the ESA defines an endangered species as “any species which is in danger of extinction throughout all or a significant portion of its range” and a threatened species as one “which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range.” Thus, we interpret an “endangered species” to be one that is presently in danger of extinction. A “threatened species,” on the other hand, is not presently in danger of extinction, but is likely to become so within the foreseeable future (that is, at a later time). In other words, the primary statutory difference between a threatened and endangered species is the timing of when a species is in danger of extinction, either presently (endangered) or in the foreseeable future (threatened).

Under section 4(a)(1) of the ESA, we must determine whether any species is endangered or threatened as a result of any one or a combination of any of the following factors: (A) the present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting its continued existence (16 U.S.C. 1533(a)(1)); 50 CFR 424.11(c). We are also required to make listing determinations based solely on the best scientific and commercial data available, after conducting a review of the species' status and after taking into account efforts, if any, being made by any State or foreign nation (or subdivision thereof) to protect the species (16 U.S.C. 1533(b)(1)(A)).

On July 5, 2022, the U.S. District Court for the Northern District of California issued an order vacating the ESA section 4 implementing regulations that were revised or added to 50 CFR part 424 in 2019 (“2019 regulations,” see 84 FR 45020, August 27, 2019) without making a finding on the merits. On September 21, 2022, the U.S. Court of Appeals for the Ninth Circuit granted a temporary stay of the district court's July 5 order. On November 14, 2022, the Northern District of California issued an order granting the government's request for voluntary remand without vacating the 2019 regulations. On April 5, 2024, the Services published a final rule revising the section 4 implementing regulations (89 FR 24300). Because the 2024 revised regulations became effective on May 6, 2024, we considered them during the development of this proposed rule. For purposes of this determination and in an abundance of caution, we considered whether the analysis or its conclusions would be any different under the pre-2019 regulations. We have determined that our analysis and conclusions presented here would not be any different.

Status Review

To determine whether each of the seven giant clam species warrants listing under the ESA, we completed a Status Review Report, which summarizes information on each species' taxonomy, distribution, abundance, life history, and biology; identifies threats or stressors affecting the status of each species; and assesses the species' current and future extinction risk. We appointed a biologist in the Office of Protected Resources Endangered Species Conservation Division to compile and complete a scientific review of the best scientific and commercial data available on the giant clam species, including information received in response to our request for information (82 FR 28946, June 26, 2017).

The Status Review Report was subject to independent peer review pursuant to the Office of Management and Budget Final Information Quality Bulletin for Peer Review (M-05-03; December 16, 2004). It was peer reviewed by four independent specialists selected from the academic and scientific community with expertise in giant clam biology, conservation, and management. The peer reviewers were asked to evaluate the adequacy, appropriateness, and application of data used in the Status Review Report, as well as the findings made in the “Assessment of Extinction Risk” section of the report. All peer reviewer comments were addressed prior to finalizing the Status Review Report and publication of this finding.

We subsequently reviewed the Status Review Report, its cited references, and peer review comments, and conclude that it synthesizes the best available scientific and commercial data related to the seven giant clam species considered here. In making our determinations, we have applied the statutory provisions of the ESA, our regulations regarding listing determinations, and relevant policies identified herein.

The Status Review Report and the peer review report are available on our website (see

ADDRESSES

section). Below is a summary of the information from the Status Review Report and our analysis of the status of the seven giant clam species.

Biological Review

Taxonomy and Species Descriptions

Giant clams are a small but conspicuous group of the planet's largest and fastest growing marine bivalves. They fall within the order Veneroida, family Cardiidae, and subfamily Tridacninae (Schneider, 1998). For many years, giant clams were considered to occupy their own family (Tridacnidae) sister to Cardiidae until molecular phylogenetics (Maruyama

et al.,

1998; Schneider & Foighil, 1999) and comparison of sperm ultrastructure (Keys & Healy, 2000) supported reclassifying the group as a subfamily within Cardiidae. This is the current, most widely accepted classification; however, Neo

et al.

(2017) note that others continue to argue that Tridacnidae should be retained as a full family based on its highly distinct

morphology (Huber & Eschner, 2011; Penny & Willan, 2014).

Colloquially described as having `upside down' orientation (Penny & Willan, 2014), giant clams lie with the hinge of their shell facing downwards, allowing their byssus (

i.e.,

filamentous threads) to attach the organism to the substrate while orienting their enlarged mantle upwards toward the sunlight (Soo & Todd, 2014). Additionally, most giant clam species have an epifaunal lifestyle (

i.e.,

situated on top of the substrate) in contrast to the largely infaunal lifestyle of their cardiid ancestors.

There are two extant genera of giant clams,

Hippopus

and

Tridacna,

which are distinguished by several shell and mantle characteristics. In

Hippopus,

a very narrow byssal orifice is bordered by interlocking teeth, while

Tridacna

exhibits a well-defined byssal gape without teeth. Additionally, when the clam is completely open, the mantle of

Tridacna

extends laterally beyond the margin of the shell, whereas the mantle of

Hippopus

does not (Lucas, 1988). A result of this difference is that

Hippopus

species tend to gape their valves further apart than

Tridacna

species, thus exposing more mantle surface area (Lucas, 1994).

There are currently 12 species of giant clams recognized in the literature, though this number changes often as advances in molecular phylogenetics resolve evolutionary relationships (including cryptic speciation) that had been overlooked by traditional morphology-based taxonomies. Joseph Rosewater's seminal work in 1965 is widely cited as the authoritative material for early descriptions of giant clam species and includes six current species that remain valid to date:

H. hippopus

(Linnaeus, 1758),

T. gigas

(Linnaeus, 1758),

T. derasa

(Röding, 1798),

T. maxima

(Röding, 1798),

T. squamosa

(Lamarck, 1819), and

T. crocea

(Lamarck, 1819). He later added

H. porcellanus

to this list after re-examining its classification (Rosewater, 1982).

At the time of the 1965 report,

T. mbalavuana

had only been formally described from fossils on Viti Levu, Fiji. However, Fijians had long known of this species occurring in local waters as `tevoro', or devil clam. Thus, when Lucas

et al.

(1991) re-discovered the species in 1991, they described it as the new species

T. tevoroa.

It was not until 2000 that

T. mbalavuana

and

T. tevoroa

were re-classified as synonymous based on morphological similarities (Newman & Gomez, 2000). As in the Status Review Report, we refer to this species by its lectotype (

i.e.,

its original classification),

T. mbalavuana.

Additionally, Richter

et al.

(2008) described a new species,

T. costata,

in 2008, but upon further analysis, it too was found to be synonymous with a previously described species,

T. squamosina,

first discovered by Rudolf Sturany (1899) during the early Austro-Hungarian expeditions of the Red Sea (Huber & Eschner, 2011). As in the Status Review Report, we refer to this species by its lectotype,

T. squamosina.

Based on the best available scientific and commercial data summarized above, we find that all seven species of giant clams (

H. hippopus, H. porcellanus, T. derasa, T. gigas, T. mbalavuana, T. squamosa,

and

T. squamosina

) are currently considered taxonomically-distinct species and, therefore, meet the definition of “species” pursuant to section 3 of the ESA. Distinguishing features of each species are summarized below.

Hippopus Hippopus

Commonly referred to as the horse's hoof, bear paw, or strawberry clam,

H. hippopus

has a heavy, thick shell that features prominent reddish blotches in irregular concentric bands (Rosewater, 1965). The shell interior is porcellaneous white, frequently flushed with yellowish orange on the ventral margin (Kinch & Teitelbaum 2010; Rosewater, 1965). Primary radial sculpture consists of 13 or 14 moderately convex rib-like folds over the surface of the valve, extending towards the ventral slope where they become obsolete (Rosewater, 1965). The mantle usually exhibits mottled patterns in green, yellow-brown or grey, and the incurrent siphon lacks guard tentacles (Neo

et al.,

2017). Juveniles and young, smaller adults are usually attached to coral rubble by their byssus, whereas older (larger, heavier) individuals are typically found unattached on the substratum being held in place by their weight (Rosewater, 1965; Neo

et al.,

2017). The largest reported shell length for

H. hippopus

is 50 cm, which was documented at the Bolinao Marine Laboratory in the Philippines (Neo

et al.,

2017).

Hippopus Porcellanus

Commonly referred to as the China clam,

H. porcellanus

grows to a maximum size of 40 cm, but is most commonly found at shell lengths of around 20 cm (Kinch & Teitelbaum, 2010). The shell exterior is off-white, occasionally with scattered weak reddish blotches. The shell interior is porcellaneous white, often flushed with orange on the ventral margin, and the mantle ranges from a yellowish-brown to a dull green or grey (Kinch & Teitelbaum, 2010). This species is distinguished from its congener,

H. hippopus,

by its smoother and thinner valves and presence of fringing tentacles at the incurrent siphon (Neo, Eckman,

et al.,

2015).

Tridacna Derasa

T. derasa,

or the smooth giant clam, is the second largest giant clam species, with a maximum size of around 60 cm (Neo

et al.,

2017).

T. derasa

has a heavy, plain-colored shell and can be distinguished from other species by its low primary and secondary radial sculpture. Primary radial sculpture consists of 7-12 broad, shallow rib-like folds (usually 6-7 main folds), and the shells are often greatly thickened at the umbos (

i.e.,

the oldest, most prominent point of the shell near the ventral margin) (Rosewater, 1965). The mantle is often characterized by elongate patterns of brilliant greens and blues, and the incurrent siphon is equipped with inconspicuous guard tentacles (Neo

et al.,

2017).

Tridacna Gigas

T. gigas

is known as the true giant clam and is the largest of all the giant clam species, growing to a maximum shell length of 137 cm and maximum weight in excess of 225 kg (Beckvar, 1981; Rosewater, 1965). The shell of

T. gigas

is thick and heavy, equivalve (having valves of the same size), and equilateral (symmetrical front-to-back) (Hernawan, 2012). The shell exterior is off-white, and is often covered with marine growths (

e.g.,

vermetids, annelid tubes, coral,

etc.

) (Kinch & Teitelbaum, 2010; Rosewater, 1965). For the most part, the shell lacks scales except near the byssal orifice where small scales may be present. The shell interior is porcellaneous white, dull in the area within the pallial line, and shiny above the pallial line to the dorsal end of the shell (Rosewater, 1965). Often, the mantle is yellowish-brown to olive-green and is a darker shade along the mantle's edge and around the clam's siphons (Rosewater, 1965). Numerous, small, brilliant blue-green rings are dispersed across the mantle, each enclosing one or several hyaline organs. These rings are especially prevalent along the lateral edges of the mantle and around the siphonal openings (Rosewater, 1965). Smaller specimens (

i.e.,

150-200 mm) may be more uniformly colored, lacking a darker shade along the edge of the mantle and with fewer colored rings (Rosewater, 1965).

T. gigas

is readily identified by many characteristics, most notably its large

size. The species can also be identified by four to six unique deep radial folds that give way to elongate, triangular projections at the upper margins of its shells (Hernawan, 2012; Lucas, 1988), a complete outer demibranch (the V-shaped structure of gills common to bivalves; Rosewater, 1965), the lack of tentacles on the inhalant siphon (Hernawan, 2012), and the lack of byssal attachment (

i.e.,

they are free-living; Rosewater, 1965).

Tridacna Mbalavuana

Before it was formally classified taxonomically, Fijians had long referred to

T. mbalavuana

as `tevoro,' or devil clam, based on its thin, sharply-edged valves and warty brownish grey mantle.

T. mbalavuana

has been hypothesized to be a transitional species between the

Hippopus

and

Tridacna

genera due to overlapping characteristics (Lucas

et al.,

1991; Schneider & Foighil, 1999). It has

Hippopus

-like features including the absence of a byssal gape, a mantle that does not extend over the shells, and the absence of hyaline organs (Lucas

et al.,

1991); however,

T. mbalavuana

looks most like

T. derasa

in appearance (Lewis & Ledua, 1988). It can be distinguished from

T. derasa

by its rugose mantle, prominent guard tentacles on the incurrent siphon, thinner valves, and colored patches on the shell ribbing (Neo, Eckman,

et al.,

2015). The shell exterior is off-white, often partly encrusted with marine growths. It can grow to just over 50 cm long (Lewis & Ledua, 1988; Neo, Eckman,

et al.,

2015) with the largest specimen recorded at 56 cm (Lucas

et al.,

1991).

Tridacna Squamosa

Commonly known as the fluted or scaly giant clam due to the characteristic leaf-like projections on its valves,

T. squamosa

is one of the most widely distributed species of giant clams. The exterior of its shell is greyish white in color, often with various hues of orange, yellow, or pink/mauve (Rosewater, 1965). The primary radial sculpture consists of 4-12 strongly convex, rib-like folds. The concentric sculpture consists of “undulate lines of growth which produce widely spaced, broadly leaf-like, projecting scales on primary folds” (Rosewater, 1965). The prominent scales on the shell commonly feature different shades or colors (Kinch & Teitelbaum, 2010). The shell interior is porcellaneous white, with an occasional hint of orange (Kinch & Teitelbaum, 2010). Rosewater (1965) describes the mantle as having a main ground color of greyish purple with a row of light blue rhomboidal spots along the outer mantle margin and multicolored irregularly-circular spots toward the center. The outer periphery of the spots is pale yellow, inside of which is a band of dark yellow, and the entire center is nearest to light blue. Generally,

T. squamosa

reaches a maximum shell length of ~40 cm (Neo

et al.,

2017).

Tridacna Squamosina

T. squamosina,

or the Red Sea giant clam, exhibits a strong resemblance to

T. squamosa,

but can be distinguished by its asymmetrical shells, crowded scutes, wider byssal orifice, and five to seven deep triangular radial folds (Roa-Quiaoit, 2005; Richter

et al.,

2008). Additionally, the mantle is most commonly a subdued brown mottled pattern with a green margin that features prominent “wart-like” protrusions and pale markings following the mantle contour (Richter

et al.,

2008). These are the main diagnostic features separating

T. squamosina

from its sympatric congeners and are conservatively present even in small clams <10 cm shell length (Richter

et al.,

2008).

T. squamosina

can reach at least 32 cm in shell length (Neo, Eckman,

et al.,

2015)—the largest specimen recorded was found in the southern Red Sea at Kamaran Island, off the coast of Yemen (Huber & Eschner, 2011).

Range, Distribution, and Habitat Use

H. Hippopus

H. hippopus

is widely distributed throughout the Indo-Pacific (

i.e.,

the tropical and subtropical waters of the Indian Ocean, the western and central Pacific Ocean, and the seas connecting the two in the general area of Indonesia), occurring from the Andaman and Nicobar Islands in the west to the Republic of Kiribati in the east, and from New Caledonia in the south to the southern islands of Japan in the north (Neo

et al.,

2017).

According to Munro (1993a),

H. hippopus

occurs in the widest range of habitat types of all the giant clam species. Most often, it is found in shallow, nearshore patches of reef, sandy areas and seagrass beds that can be exposed during low tides, but it can also be found on reefs as deep as 10 m (S. Andréfouët, pers. obs. cited in Neo

et al.,

2017). Based on a recent survey in New Caledonia, Purcell

et al.

(2020) found that

H. hippopus

“strongly preferred” lagoonal reefs. The authors hypothesized that the species may either prefer the siltier sediments and more turbid water of lagoon reef flats or alternatively may have low tolerance to the wave exposure of barrier reefs.

H. Porcellanus

H. porcellanus

has one of the most restricted geographic ranges of the giant clams, centered in the Coral Triangle region. The species is mostly known from the Sulu Archipelago and Palawan region in the Philippines, but it has also been reported in Palau, the Milne Bay Province (Papua New Guinea), Sabah (Malaysia), and Sulawesi and Raja Ampat (Indonesia) (S. Wells, 1997; Neo

et al.,

2017).

There is very little information specifying the habitat preferences of

H. porcellanus,

but according to Calumpong (1992), the species is commonly found in shallow, nearshore sandy areas adjoining coral reefs. Juvenile or young

H. porcellanus

are frequently found byssally attached to coral heads, whereas larger mature

H. porcellanus

can be found on sandy bottoms unattached to substrate (Rosewater, 1982; Kinch & Teitelbaum, 2010).

T. Derasa

The geographic range of

T. derasa

primarily encompasses the Coral Triangle region, although it extends east to Tonga and as far west as the Cocos (Keeling) Islands in the eastern Indian Ocean (Rosewater, 1965). Adams

et al.

(1988) described

T. derasa

as having a patchy distribution, being rare in many places throughout its range and abundant in others. Notably,

T. derasa

has been one of the most widely cultured species of giant clam and has been introduced to a number of countries and territories throughout the central and western Pacific Ocean. This includes the Federated States of Micronesia (FSM), Marshall Islands, Tuvalu, Cook Islands, Samoa, and American Samoa.

T. derasa

preferentially inhabits clear offshore waters distant from areas of significant freshwater run-off (Munro, 1993a). According to Calumpong (1992), the species appears to favor oceanic environments (

i.e.,

small islands and atolls) more than fringing reefs adjacent to large island masses. The species is known to occur at depths of 4-25 m (Lewis

et al.,

1988; Neo

et al.,

2017), and is usually found weakly attached to the tops and sides of coral outcrops as juveniles, but may become detached upon reaching a larger size (Adams, 1988).

T. Gigas

The natural range of

T. gigas

spans the shallow waters of the Indo-Pacific and the Great Barrier Reef, from Myanmar in the west to the Republic of Kiribati in the east, and from the Ryukyus Islands

of southern Japan in the north to Queensland, Australia in the south (bin Othman

et al.,

2010; Neo

et al.,

2017). Cultured specimens of

T. gigas

have been introduced in American Samoa, the Cook Islands, Hawaii, and Samoa (Neo

et al.,

2017). Like most other giant clam species,

T. gigas

is typically associated with coral reefs and can be found in many habitats, including high- and low-islands, atoll lagoons, and fringing reefs (Munro, 1993a). In a broad survey of

T. gigas

distribution throughout the Great Barrier Reef, Braley (1987a) found that the species was most common on inshore reefs potentially influenced by seasonal fluctuations in salinity and turbidity and was rare south of 19° S. The observed distribution was essentially opposite of that for

T. derasa,

which was found primarily on offshore reefs and was common in the Swain Reefs at 21-22° S. These contrasting distributions led Braley (1987b) to the conclusion that temperature may limit the distribution of young

T. gigas,

while

T. derasa

may be more sensitive to salinity and/or turbidity.

T. gigas

is typically found between the depths of 2 to 20 m and is often found among

Acropora

spp. or other hard coral communities, hard reef substrata, or on bare sand (Braley, 1987b; Kinch & Teitelbaum 2010; Rosewater, 1965).

T. Mbalavuana

T. mbalavuana

has one of the most restricted distributions of all the giant clam species. For many years, it had only been observed in Fiji and Tonga, but recent reports indicate that this species may be found in low numbers outside of these two locations. According to Kinch and Teitelbaum (2010),

T. mbalavuana

had been observed in the Loyalty Islands in New Caledonia, a report later supported by Tiavouane and Fauvelot (2016), who encountered two individuals on the northeastern barrier reef of New Caledonia after “exhaustive searches” (Neo

et al.,

2017). Single individuals were also reportedly observed on Lihou Reef in the Coral Sea (Ceccarelli

et al.,

2009) and in the Raja Ampat region of West Papua, Indonesia (Wakum

et al.,

2017), but neither of these reports have been further corroborated.

In Fiji, individuals are most often observed along outer slopes of leeward reefs in the eastern Lau Islands, in very clear, oceanic water (Ledua

et al.,

1993). In Tonga, they are found in the northern Vava`u and Ha`apai islands.

T. mbalavuana

has a deeper depth distribution than most other giant clam species. In one study on spawning and larval culture of

T. mbalavuana,

individuals were collected from waters of Fiji and Tonga (Ledua

et al.,

1993). The mean depth of clams collected in Fiji was 27.4 m, with samples collected from depths ranging from 20 to 33 m, and all specimens were found on the leeward side of reefs and islands. Many of the clams found in Tonga were next to the edge of a sand patch and cradled against rocky outcrops, rubble or bare rock with steep slopes (Ledua

et al.,

1993).

T. Squamosa

T. squamosa

is the second-most widely distributed giant clam species, with a broad geographic range that extends from the Red Sea and eastern Africa in the west to the Pitcairn Islands in the east, and from the Great Barrier Reef in the south to southern Japan in the north (bin Othman

et al.,

2010; Neo

et al.,

2017). The species has also been introduced in Hawaii and Guam (CITES, 2004b).

T. squamosa

is usually found on coral reefs or on adjacent sandy areas (Neo

et al.,

2017). Juveniles are often attached to the substrate by a “weak but copious byssus,” while adults can be found either attached or free-living (Neo

et al.,

2017; Rosewater, 1965).

T. squamosa

occurs across a broad depth range, which includes shallow reef flats, patch reefs, and reef slopes, both inside and outside of lagoons. Individuals have been observed as deep as 42 m in the Red Sea (Jantzen

et al.,

2008).

T. squamosa

is typically more common on shelving fringing reefs than reef flats (Govan

et al.,

1988) and seems to prefer sheltered environments (Kinch & Teitelbaum, 2010; Munro, 1993a). Comparing the distribution of

T. squamosa

and

T. maxima

in Mauritius, Ramah

et al.

(2017) found that

T. squamosa

were most often attached to flat substrata, such as dead plate corals or rubble. Hardy and Hardy (1969) reported that

T. squamosa

and

H. hippopus

occupied much the same habitat in Palau, both being widely distributed in relatively shallow water in the lagoon and on the barrier and fringing reefs; although,

T. squamosa

was reportedly more commonly associated with coral areas of

Acropora

spp. than adjacent sandy areas. In New Caledonia, Purcell

et al.

(2020) interpreted the relatively high abundance of

T. squamosa

on barrier reef sites compared to lagoonal reefs as indication that the species may prefer cleaner waters, as opposed to the siltier sediments and more turbid seawater of lagoon reef flats. However, Lewis

et al.

(1988) note that the species is more tolerant of turbid water than

T. derasa.

Paulay (1987) reported that all observations of

T. squamosa

in the Cook Islands were from the outer reef slope, occasionally to depths of 30 m or more.

T. Squamosina

T. squamosina

is endemic to the Red Sea, with its past and present distribution including the northeastern Gulf of Aqaba, the Sinai coast, and eastern coast of the Red Sea down to Yemen (Huber & Eschner, 2011; Lim

et al.,

2021; Richter

et al.,

2008; Rossbach

et al.,

2021). There have also been several anecdotal accounts of the species in Mozambique; however, later evidence of genetic divergence between specimens in the Red Sea and Mozambique (Moreels, 2018), as well as the significant geographic distance from its central range, suggests that the reported sightings may be of its recently-resurrected sister species,

T. elongatissima,

with which it shares a close phylogenetic history (Fauvelot

et al.,

2020; Tan

et al.,

2021). For this reason, without more information to verify these anecdotal sightings, we do not include the Western Indian Ocean in the natural range of

T. squamosina.

In a survey of giant clams in the Red Sea, Richter

et al.

(2008) noted that live specimens of

T. squamosina

were found exclusively in very shallow water habitats (

e.g.,

reef flats, rocky and sandy-rubble flats, seagrass beds, or under branching corals or coral heads shallower than 2m). Thus, unlike the other two Red Sea species (

T. maxima

and

T. squamosa

), which have broad depth distributions,

T. squamosina

is restricted to the reef top and is usually weakly attached to the substrate (Richter

et al.,

2008).

Diet and Feeding

During the earliest stages of larval development, giant clams initially rely on nutrients stored in the egg yolk. Upon formation of the velum and hollow intestines within the first 2-3 days after fertilization, veliger larvae transition to planktivory and are able to actively ingest flagellates (~5 μm in diameter), zooxanthellae and dissolved organic nutrients from the seawater via the mouth (Fitt

et al.,

1984; Soo & Todd, 2014). Like most bivalves, giant clams retain the ability to filter feed into adulthood by pumping water into their mantle cavities via an inhalant siphon, filtering plankton through ciliated gills, and passing the filtered water back out via an excurrent siphon (Hardy & Hardy, 1969).

However, a defining characteristic of giant clams is their mutualistic relationship with dinoflagellates of the family Symbiodiniaceae, known commonly as zooxanthellae, which

provide the primary source of nutrition to adult clams. Giant clams strictly acquire symbiotic algae from the seawater during larval development and therefore do not inherit symbionts via parental oocytes (Fitt & Trench, 1981; Hartmann

et al.,

2017). Furthermore, zooxanthellae are housed extracellularly within a diverticular extension of the digestive tract (Norton

et al.,

1992). This `tubular system' extends throughout the upper levels of the mantle and is arranged as a dense network of tertiary canals branching off of secondary structures with no direct connection to the haemolymph of the clam (Norton

et al.,

1992). Detailed scanning electron microscope images have shown that zooxanthellae are often stacked in pillars within these canals and are co-located with light-scattering iridocyte cells that enhance photosynthesis (L. Rehm, unpub.) and protect the algal cells from damaging UV radiation (Rossbach, Overmans,

et al.,

2020; Rossbach, Subedi,

et al.,

2020).

Symbiosis is thought to be established during metamorphosis from pediveliger to the juvenile clam. At this point, zooxanthellae can be observed migrating from the stomach to the tubular system (Fitt

et al.,

1986; Norton

et al.,

1992). Although, more recent studies have shown that genes known to be associated with symbiosis and glycerol synthesis are expressed in giant clam larvae, suggesting that symbiotic activity may be initiated earlier during larval development (Mies

et al.,

2016; Mies, Voolstra,

et al.,

2017).

Giant clams receive the majority of their metabolic carbon requirements via symbiotic autotrophy. They provide dissolved inorganic nutrients to support photosynthesis (

e.g.,

, NO

, PO

) via direct absorption from the seawater and as an excretory byproduct of respiration (Hawkins & Klumpp, 1995; Toonen

et al.,

2011). In return, zooxanthellae transfer photosynthetic carbon to the host in the form of glucose, glycerol, oligosaccharides and amino acids (Griffiths & Streamer, 1988; Ishikura

et al.,

1999; Mies

et al.,

2016).

Under natural conditions, the contribution of autotrophy to giant clam nutrition tends to increase with body size and has been shown to vary between species (Klumpp & Griffiths, 1994; Klumpp & Lucas, 1994; Hawkins & Klumpp, 1995). This may in part be related to differences in their characteristic habitats. For example,

T. derasa

and

T. mbalavuana,

two species which occur predominantly in clear, oceanic environments, derive most (

T. mbalavuana:

70 percent at 28 m, 105 percent at 15 m), if not all (

T. derasa

), of the carbon required for growth and respiration from autotrophy (Klumpp & Lucas, 1994). Notably, only

T. mbalavuana,

which is the deepest-occurring species of giant clam, increased its photosynthetic efficiency in the lowest light conditions (Klumpp & Lucas, 1994).

H. hippopus

and

T. gigas

exhibit a different strategy altogether, reflecting their natural occurrence in shallower intertidal and subtidal habitats, where there is often a higher concentration of suspended organics in the water column. Klumpp

et al.

(1992) showed that

T. gigas

is an efficient filter-feeder and that heterotrophic carbon supplied significant amounts of the total carbon necessary for its respiration and growth (65 percent in ~43 mm individuals and 34 percent in ~167 mm individuals). In a follow-up study, Klumpp and Griffiths (1994) similarly found that ingested carbon provided 61 to 113 percent of total needs in 40 to 80 mm

T. gigas

and 36 to 44 percent in

H. hippopus.

Some have hypothesized that differences in energy acquisition and expenditure may in part explain the growth and size differences among giant clam species, and in particular the enormous size of

T. gigas.

At this point, however, no clear nutritional basis for these differences has been resolved (Klumpp & Griffiths, 1994).

Giant clams associate with several Symbiodiniaceae genera, which can vary by geographic location (Fitt

et al.,

1986). In the central Red Sea, for example, all sampled species (

T. maxima, T. squamosa, T. squamosina

) were found to exclusively harbor strains of

Symbiodinium

(formerly known as clade A) (Pappas

et al.,

2017). In Okinawa, Japan,

T. squamosa

hosted varying communities of

Symbiodinium, Cladocopium

(formerly clade C), and

Durusdinium

(formerly clade D) (Ikeda

et al.,

2017). Similarly, populations of

T. squamosa, T. maxima,

and

T. crocea

in eastern Indonesia were found to associate with mixed communities of these three genera (DeBoer

et al.,

2012). While certain symbiont genera have been shown to confer physiological benefits to coral hosts (

e.g.,

greater tolerance to thermal stress or enhanced growth rate), there is no consistent evidence that these patterns translate directly to giant clams (reviewed in DeBoer

et al.,

2012).

Growth and Reproduction

Giant clams are protandrous hermaphrodites, meaning they mature first as males and later develop ovaries to function as both male and female simultaneously (Wada, 1952; Rosewater, 1965). Size and age at maturity vary by species and geographic location, but generally, giant clams are known to reach male phase maturity at around 2-3 years of age (Heslinga

et al.,

1984; Shelley, 1989) and female phase maturity as early as 3-5 years (Heslinga

et al.,

1984; Isamu, 2008). In larger species, such as

T. gigas,

female maturity typically occurs later at around 8-9 years of age (Gomez & Mingoa-Licuanan, 2006). Giant clams reproduce via broadcast spawning, in which sperm and eggs are released into the water column where external fertilization takes place (Wada, 1954). Sperm is released first, followed by eggs after a short interval (Munro, 1993a).

Giant clams are exceptionally fecund, with individuals producing by many estimates tens to hundreds of millions of eggs during a single spawning event (Lucas, 1988). This number varies by species; for example, estimates suggest that

H. porcellanus

can release around 5 million eggs (Alcázar

et al.,

1987),

H. hippopus

can release 25-60 million eggs (Jameson, 1976; Alcala

et al.,

1986), and

T. gigas

can release up to 500 million eggs (Crawford

et al.

1986). However, despite their high fecundity, giant clams experience very high rates of mortality during early development (Jameson, 1976; Beckvar, 1981), resulting in very low levels of natural recruitment (Munro, 1993a). Reports suggest that less than 1 percent of all giant clam fertilized eggs survive larval development and progress to the juvenile phase in the wild (Jameson, 1976; Fitt

et al.,

1984; Crawford

et al.,

1986). As Lucas (1994) describes, “the extreme example is

T. gigas,

which being at or near the pinnacle of fecundity, must have near the lowest level of survival of potential recruits in the animal kingdom.”

Many have described giant clam recruitment as “erratic” (McKoy

et al.,

1980; Adams

et al.,

1988; Lucas, 1994; Guest

et al.,

2008). For example, Braley (1988) observed “extremely low” average recruitment on the Great Barrier Reef, punctuated by a major recruitment event in 1987, which yielded the largest population of

T. gigas

that had been recorded at the time. This pattern aligns with the concept of `sweepstakes' reproduction, which is the chance matching of reproductive activity with oceanographic conditions conducive to spawning, fertilization, dispersal, and successful recruitment (Hedgecock, 1994). This can lead to sporadic waves of recruitment depending on the prevailing oceanographic conditions facilitating fertilization and carrying a successful cohort of `sweepstakes' larvae to a suitable settlement location. Importantly, for broadcast spawning organisms like giant clams, which

primarily rely on the mixing of gametes with neighboring individuals, this reproductive strategy can be especially sensitive to changes in population density. In particular, low abundance and low population density severely reduces the likelihood of such sweepstakes success by minimizing the chance of fertilization.

There is considerable variation in the frequency and seasonality of spawning events among giant clam species. There is no evidence of reproductive seasonality in the central tropics, with some populations possessing ripe gametes year-round (Heslinga

et al.,

1984; Munro, 1993a; Lindsay

et al.,

2004). At higher latitudes, spawning is most often associated with late spring and summer months and can occur once per year (Shelley & Southgate, 1988) or in some cases periodically over the course of several months (Fitt & Trench, 1981; Heslinga

et al.,

1984; Roa-Quiaoit, 2005). The environmental cues that initiate gamete release are not fully understood, but there is evidence that the lunar cycle may play a critical role. In Palau, for example, 76 percent and 24 percent of 55 observed spawning events by

T. gigas

occurred during the second and fourth quarter of the lunar cycle, respectively (Heslinga

et al.,

1984). Unlike many other broadcast spawning organisms, there is little evidence that temperature is important for the induction of spawning (Wada, 1954; Fitt & Trench, 1981).

Once one or more clams have begun to spawn, chemical cues associated with egg release have been shown to play a role in triggering the spawning of nearby individuals, which then release sperm for fertilization (Munro, 1993a). While a maximum distance between spawning individuals has not been quantified (Neo

et al.,

2015), in situ observations by Braley (1984) showed that 70 percent of the nearest spawning neighbors were within 9 m of one another, while only 13 percent were between 20-30 m of one another. Through laboratory trials, Neo

et al.

(2015) found that gametes of

T. squamosa

remained viable for up to 8 hours, but that viability decreased significantly with time. Because of these factors, maintaining sufficient population densities to facilitate fertilization among neighboring individuals is vital to the persistence of giant clam populations.

Importantly, there is also some evidence that giant clams are able to self-fertilize with varying fitness consequences among different species. After observing that the end of sperm release occasionally overlaps with the beginning of egg release in certain giant clam species (see also Kurihara

et al.

(2010)), Murakoshi and Hirata (1993) experimentally induced self-fertilization in four species of giant clams (

H. hippopus, T. crocea, T. maxima,

and

T. squamosa

) by removing the gonads and mixing gametes. They found that all four species are capable of self-fertilization, but that larval development of

H. hippopus

was significantly altered, and no

T. maxima

juveniles metamorphosed completely to the normal pediveliger stage. Juvenile

T. crocea

and

T. squamosa

survived up to a year post-fertilization, but the study was not long enough to evaluate possible effects on reproductive maturity or later-phase development. More recently, Zhang

et al.

(2020) evaluated the fitness effects of self-fertilization in three species of giant clams (

T. crocea, T. derasa,

and

T. squamosa

) after 1 year of development. They found that there was no effect of self-fertilization on the fertilization rate or zygotic fertility in any species. Larval survival and growth rate was significantly reduced in

T. crocea

and

T. squamosa,

but not

T. derasa.

However, while self-fertilization may be possible in some species, numerous accounts of spawning in culture and in situ suggest that sperm and eggs are released successively without an overlap in timing in the vast majority of spawning events (LaBarbera, 1975; McKoy, 1980; Wada, 1954). It is likely that this limits the occurrence of self-fertilization in nature and minimizes its role in giant clam productivity.

Once an egg is fertilized, the life cycle of giant clams is typical of bivalve molluscs (Lucas, 1994; Soo & Todd, 2014). Fertilized eggs are approximately 90-130 μm in diameter (Jameson, 1976) and have a slight negative buoyancy. They usually develop into swimming trochophores within 12-24 hours, at which time they are able to alter their depth distribution and begin searching for an eventual settlement site (Ellis, 1997; Neo

et al.,

2015). Shell production in molluscs begins at this early phase of development, following a thickening of epithelial cells that will define the future shell field (Gazeau

et al.,

2013). Within 36-48 hours after fertilization, larvae develop into shelled, swimming veligers, which use a ciliated velum for locomotion and feeding (Soo & Todd, 2014). The veligers are highly motile and begin feeding on microalgae of up to 10 μm in diameter (Munro, 1993a). Over the course of several days, the velum begins to degenerate and a foot develops as the larvae transition into the pediveliger stage (Soo & Todd, 2014). At this point, larvae alternate between swimming and crawling on the substrate, using their foot for sensing and feeding (Lucas, 1988; Soo & Todd, 2014). Pediveligers generally develop 6-14 days post-fertilization; however, Fitt and Trench (1981) noted considerable variation in the timing of this transition, where most took place by day 10 but others were observed up to 29 days post-fertilization.

Larvae metamorphose into juvenile clams at an approximate size of 200 μm (LaBarbera, 1975; Lucas, 1988; Soo & Todd, 2014). Juvenile clams remain mobile and are able to crawl both horizontally and vertically using their foot as they search for a settlement location (Soo & Todd, 2014). Giant clam larvae tend to settle on substrates that offer shelter in the form of grooves and crevices, highlighting the importance of habitat rugosity during this stage of development (Soo & Todd, 2014). Additionally, juveniles have been observed to move non-randomly and clump towards conspecifics, which some hypothesize may be a behavioral adaptation to enhance reproduction and predator defense (Huang

et al.,

2007; Neo, 2020). Juvenile clams eventually attach themselves to the substrate by use of byssal threads, which in some species will remain in place throughout their lifetime. Larger species typically lose the byssal threads after reaching adulthood and are held in place by their size and weight (Lucas, 1988).

Growth rates vary among species, with larger species exhibiting more rapid growth than smaller species (Munro & Heslinga, 1983; Lucas, 1988). Growth rates after settlement generally follow a sigmoid (“S” shaped) curve, beginning slowly, then accelerating after approximately 1 year and slowing again as the animals approach sexual maturity (Lucas, 1988; Ellis, 1997). Lucas (1994) provides examples of maximum rates of monthly shell growth for several species as recorded under culture conditions in the Philippines:

H. hippopus

—5.3 mm,

T. squamosa

—4.5 mm,

T. derasa

—5.6 mm, and

T. gigas

—9.1 mm (Calumpong, 1992; Gomez & Mingoa, 1993). Shell growth continues throughout the clam's lifespan (Lucas, 1994).

The maximum lifespan of giant clams is not known, but the oldest reliably aged individual was a large

T. gigas

determined to be 63 years old (Lucas, 1994). Similar aging studies based on the analysis of growth rings in the shell estimated a 43 cm-long

T. squamosa

to be around 22 years old (Basker, 1991), a ~20 cm-long

T. maxima

to be around 28 years old (Romanek

et al.,

1987), and a 93 cm-long

T. gigas

to be around 60 years old (Watanabe

et al.,

2004). Using growth and mortality estimates, Dolorosa

et al.

(2014) predicted a

lifespan of more than 20 years for

H. porcellanus.

Population Structure

Current literature indicates several consistent features of giant clam population genetics throughout their range. The first is significant genetic differentiation between giant clam populations of the central Pacific region, including Kiribati, Marshall Islands, Tuvalu and Cook Islands, and the western Pacific region, including the Great Barrier Reef, Philippines, Solomon Islands and Fiji (Benzie & Williams, 1995, 1997). The pattern is consistent across

T. gigas

and

T. maxima,

although there is some variability in the inferred level of connectivity between the Great Barrier Reef and Philippines in

T. derasa

(Macaranas

et al.,

1992). Interestingly, the patterns of genetic connectivity do not reflect oceanic currents as would be expected for a passively-dispersing organism like giant clams. Hence, Benzie and Williams (1997) hypothesize that “other mechanisms dominate present-day dispersal, or that [the observed patterns] reflect past connectivity which present-day dispersal along major surface currents has not altered over thousands of years.”

Other studies describe a relatively consistent pattern of genetic structure within the Indo-Pacific region, often highlighting four or five genetic clusters distinguishing populations of the Red Sea, Western Indian Ocean, Eastern Indian Ocean, Indo-Malay Archipelago, and Western Pacific. In every case, populations of

T. squamosa

and

T. maxima

in the Red Sea are found to be highly divergent from all other populations in their range (Nuryanto & Kochzius, 2009; Huelsken

et al.,

2013; Hui

et al.,

2016; Pappas

et al.,

2017; Lim

et al.,

2018). The same is true of Western Indian Ocean populations, though to a slightly lesser extent (Hui

et al.,

2016; Lim

et al.,

2018). Additionally, there is a uniform pattern of differentiation between giant clam populations in the Indo-Malay Archipelago and those in the eastern Indian Ocean and Java Sea (Kochzius & Nuryanto, 2008; Nuryanto & Kochzius, 2009; Huelsken

et al.,

2013; Hui

et al.,

2016). This pattern is largely consistent across

T. squamosa, T. maxima,

and

T. crocea,

although some studies note variability between species with respect to certain genetic breaks identified in the Java Sea and in Chendewasih Bay (Nuryanto & Kochzius, 2009; Huelsken

et al.,

2013). Population genetic data from

T. maxima

and

T. crocea

(species which are not subject to this rulemaking) suggest that there may also be genetic breaks between the western Pacific islands and Indo-Malay Archipelago (Nuryanto & Kochzius, 2009; Huelsken

et al.,

2013; Hui

et al.,

2016). However, similar data are not available for any of the seven species considered here.

On a smaller scale, giant clam populations within the northern and central Great Barrier Reef exhibit high genetic connectivity (Benzie & Williams, 1992, 1995, 1997). Evans and Jerry (2006) found tenuous evidence of isolation-by-distance in this region, which would suggest that populations may be connected by the prevailing southward flow of the East Australian Current. In contrast, Kittiwattanawong

et al.

(2001) found that

T. squamosa

in the Andaman Sea are genetically distinct from those in the Gulf of Thailand, likely due to the physical barrier of the Malay Peninsula minimizing dispersal between these populations.

Current and Historical Distribution and Population Abundance

There are no current or historical estimates of global abundance for any of the seven giant clam species considered here. Therefore, we rely on the best available scientific and commercial data, including formal and informal survey data, qualitative descriptions of abundance or population trends, and anecdotal reports from specific sites, to evaluate the status of each species in each country, territory, or region throughout its range.

Much of the information used to determine the status of each species is derived from Table 4 of Neo

et al.

(2017), which we have supplemented or revised based on more recent survey data or reports. We have also adjusted the criteria used to define each qualitative abundance category, which Neo

et al.

(2017) had previously defined as follows: Abundant: >100 individuals (ind) ha

-1

, Frequent: 1-10 ind ha

-1

, Rare: <0.1 ind ha

-1

. In doing so, we considered the reproductive ecology of giant clams, and in particular, the observations of Braley (1984) regarding the distance between nearest-spawning

T. gigas

during a natural spawning event. Braley (1984) measured that 70 percent of nearest-spawning individuals were within 9 m of one another, while only 13 percent were between 20-30 m of one another, suggesting that spawning synchrony decreases with distance. As broadcast spawning organisms, giant clams rely on sufficient population density in order to facilitate successful external fertilization of their gametes. Based on the distances above, we determined the minimum population density in a 1-hectare (10,000 m

) square grid in which individuals could be evenly spaced at 9 and 30 m apart. Respectively, these distances represent populations that we consider to be “Abundant,” where we expect relatively high reproductive success, and “Frequent,” where we expect lower but moderate reproductive success. A “Rare” population in which individuals are spaced farther than 30 m apart on average is likely to have infrequent, sporadic reproductive success. This approach led to the following criteria: Abundant: >100 ind ha

-1

(9-m distance), Frequent: 10-100 ind ha

-1

(30-m distance), and Rare: <10 ind ha

-1

(>30-m distance).

Importantly, precise quantitative assessments of abundance are not possible in most instances, as many regions lack current or comprehensive survey data (see the accompanying Status Review Report for all reported estimates of population density from specific surveys). Thus, where survey data are limited to only a few sites or where recent survey data are not available, we also take into account other available information, including qualitative descriptions of abundance or population trends, to reach a determination on the likely status of the species throughout each country, territory, or region in its entirety. In other words, although survey data from a single site may indicate a relatively abundant population, if the species is considered absent from all other areas, the species may be considered “frequent” or “rare” on average in that location. This methodology generally follows the approach used by Neo

et al.

(2017).

Additionally, it is important to note that, in the interest of simplicity, these qualitative abundance categories are based on an assumption of uniform spacing between individuals. However, a number of studies report that giant clams often occur in a clumped distribution, where individuals are concentrated in a number of small, distantly-separated groups. In these cases, the abundance categories may underestimate the productivity of the respective population. In other words, if survey data indicate that a species occurs in some location at low abundance on average, reproductive success is more likely if the individuals are clustered in a few small groups, minimizing the distance between neighboring individuals, than if they are spread uniformly across the seafloor.

In table 1 below, we summarize the status of each species in each of the locations where it has been observed. Full narrative descriptions of the data

and scientific studies that informed the following abundance assessments can be found in the accompanying Status Review Report (Rippe

et al.,

2023).

Table 1—Summary of the Population Status for Each of the Seven Giant Clam Species in All Countries, Territories, and Regions Where They Have Been Observed (Adapted From Neo

et al.,

2017 and Supplemented With More Recent Information Where Available)

Location

TMB

TSI

Red Sea:

Djibouti

Egypt

Israel

Jordan

Saudi Arabia

+++

Somalia

Sudan

Yemen

Southeast Africa:

Cargados Carajos Archipelago

Comoros

Kenya

Madagascar

Mauritius

Mayotte

Mozambique

La Réunion

Seychelles

South Africa

Tanzania

Indian Ocean:

India

Australia (NW Islands)

Christmas Island

−

Cocos (Keeling) Islands

−

Chagos

Maldives

Sri Lanka

East Asia:

Japan

Taiwan

−

China

−

South China Sea

South Asia:

Indonesia

+++

Malaysia

+++

Myanmar (Burma)

Cambodia

Brunei

Philippines

Singapore

−

Thailand

−

Vietnam

East Timor

Pacific Ocean:

Australia (Great Barrier Reef)

Fiji

REIN

New Caledonia

−

Papua New Guinea

Solomon Islands

+++

Vanuatu

REIN

FSM

INT

REIN

Guam

REIN

Republic of Kiribati

Marshall Islands

INT

CNMI

REIN

−

Palau

American Samoa

REIN

INT

Cook Islands

INT

French Polynesia

Pitcairn Islands

Niue

Samoa

REIN

INT

Tokelau

Tonga

REIN

Tuvalu

INT

−

United States (Hawaii)

INT

United States (Johnston Atoll)

United States (Kingman Reef)

United States (Wake Atoll)

Wallis and Futuna Islands

+++

Note:

Species abundance categories are as follows. +++: Abundant (>100 ind ha

-1

), ++: Frequent (10-100 ind ha

-1

), +: Rare (<10 ind ha

-1

), −: Locally extinct,

INT:

Introduced to non-native location;

REIN:

Reintroduced (cultured specimens) to locations where the species had previously been extirpated;

dd:

Data Deficient (

i.e.,

reports of species presence are not confirmed). Empty cells indicate locations where a species has not been observed.

Species names are abbreviated as follows: HH:

H. hippopus,

HP:

H. porcellanus,

TD:

T. derasa,

TG:

T. gigas,

TMB:

T. mbalavuana,

TS:

T. squamosa,

TSI:

T. squamosina.

Extinction Risk Analysis

Methods

In determining the extinction risk of each species, it is important to consider both the demographic risks facing the species, as well as current and potential threats that may affect the species' status. To this end, the status review synthesized the best available scientific and commercial data regarding the five threat categories listed in section 4(a)(1) of the ESA. These are: (1) the present or threatened destruction, modification, or curtailment of its habitat or range; (2) overutilization for commercial, recreational, scientific, or educational purposes; (3) disease or predation; (4) inadequacy of existing regulatory mechanisms; or (5) other natural or manmade factors affecting its continued existence. Second, we conducted a demographic risk analysis following the Viable Population (VP) approach derived from McElhany

et al.

(2000), which addresses four biological descriptors of species status: abundance, productivity (

i.e.,

population growth rate), spatial distribution, and diversity. The VP approach reflects concepts that are well-founded in conservation biology and considers demographic factors that individually and collectively provide strong indicators of extinction risk. It is designed to both capture the biological symptoms of past threats that have contributed to the species' current status and provide insight into how the species may respond to present and future threats.

With respect to each threat and each demographic risk factor, we assigned a qualitative score from 1 to 5 representing its estimated contribution to the species' extinction risk (“very low,” “low,” “moderate,” “high,” or “very high” risk). Detailed definitions of these risk levels can be found in the accompanying Status Review Report. We also assigned a confidence rating from 0 to 3, reflecting the quantity and quality of information used to assign the score, as follows: 0 = No confidence (

i.e.,

no available information); 1 = Low confidence (

i.e.,

very limited available information); 2 = Medium confidence (

i.e.,

some reliable information available, but reasonable inference and extrapolation is required); 3 = High confidence (

i.e.,

reliable information with little or no extrapolation or inference required).

Lastly, all information from the threats assessment and demographic risk analysis was synthesized to estimate the overall risk of extinction for each species. For this analysis, we used three reference levels of extinction risk (“low,” “moderate,” and “high”), which are consistent with those used in prior ESA status reviews. “Low” risk indicates a species that is not at a moderate or high level of extinction risk (see “Moderate” and “High” risk below). A species may be at a low risk of extinction if it is not facing threats that result in declining trends in abundance, productivity, spatial structure, or diversity. A species at low risk of extinction is likely to show stable or increasing trends in abundance and productivity with connected, diverse populations. “Moderate” risk indicates a species that is on a trajectory that puts it at a high level of extinction risk in the foreseeable future (see “High” risk below). A species may be at moderate risk of extinction due to projected threats or declining trends in abundance, productivity, spatial structure, or diversity. “High” risk indicates a species that is at or near a level of abundance, productivity, spatial structure, and/or diversity that places its continued persistence in question. The demographics of a species at such a high level of risk may be highly uncertain and strongly influenced by stochastic or depensatory processes. Similarly, a species may be at high risk of extinction if it faces clear and present threats (

e.g.,

confinement to a small geographic area; imminent destruction, modification, or curtailment of its habitat; or disease epidemic) that are likely to create present and substantial demographic risks.

Importantly, these extinction risk categories are not meant to be a direct translation of the final listing determination for the species, as listing determinations must also consider ongoing conservation efforts of any State, foreign nation, or political subdivision thereof (16 U.S.C. 1533(b)(1)(A)) to determine whether the species meets the ESA's definition of an “endangered species” or “threatened species.” Rather, the extinction risk assessment in the Status Review Report represents the scientific conclusion about the overall risk of extinction faced by the species under present conditions and in the foreseeable future based on an evaluation of the species' demographic risks and assessment of threats.

Defining the “Foreseeable Future”

The appropriate time horizon for evaluating whether a species is more likely than not to be at a high level of risk in the “foreseeable future” varies on a case-by-case basis. For example, the time horizon may reflect certain life history characteristics (

e.g.,

long generation time or late age-at-maturity) and the time scale over which identified threats are likely to impact the biological status of the species. In other words, the foreseeable future represents the period of time over which we can reasonably determine that both future threats and the species' response to

those threats are likely.

See generally

50 CFR 424.11(d). It does not necessarily need to be limited to the period that the species' status can be quantitatively modeled or predicted within predetermined limits of statistical confidence. Reliable projections may be qualitative in nature.

With these criteria in mind, we determined that the “foreseeable future” for the following extinction risk analyses spans approximately ~50-60 years. Based on what is known about the life history traits of giant clams, with longevity estimated to be at least 50 years (up to 60 years for

T. gigas

), maturity ranges from 3 to 9 years, and exceedingly low recruitment, it would likely take at least this amount of time (

i.e.,

multiple generations) for the effects of any management actions to be realized and reflected in population abundance indices. Similarly, the impact of present threats to the species would be realized in the form of noticeable population declines within this timeframe, as has been demonstrated in the available literature. As the primary operative threats to giant clams are overutilization for subsistence and commercial harvest, this timeframe would allow for reliable predictions regarding the impact of current levels of harvest-related mortality on the biological status of all the species.

One important exception to this timeframe is in regard to the future impacts and threats related to climate change. Based on the current standard for climate projections, under which most available models are extended to the end of the century, we use the same timeframe (

i.e.,

present day-2100) to define the “foreseeable future” in assessing the likely future threat of climate-related habitat degradation and climate-related impacts to giant clam fitness.

Threats Assessment

Below, we describe the natural and anthropogenic threats to each of the seven giant clam species within the framework of the five threat categories outlined in section 4(a)(1) of the ESA. Because a number of species occupy overlapping ranges and often co-occur in similar habitats, certain threats may apply to more than one species. In each section, we highlight the severity of the threat to each of the species affected and provide additional species-specific information where appropriate. Additional details may be found in the Status Review Report (Rippe

et al.,

2023).

The Present or Threatened Destruction, Modification, or Curtailment of Its Habitat or Range

As is mentioned in the species descriptions above, giant clams are often closely associated with coral reefs, inhabiting all types of shallow-water reef ecosystems (

i.e.,

fringing, barrier and atoll reefs), as well as various reef-adjacent habitats. However, there is no conclusive evidence that giant clams directly rely on live, pristine corals for their survival. Certain species are habitat generalists (

e.g., T. squamosa, T. gigas

)—they are often observed among live corals but can also be found in other habitats, which are not pristine coral reef (

e.g.,

sand, rock, dead coral rubble, seagrass beds, macroalgae zones). Others are more specialized—

T. mbalavuana

is found exclusively at depth on reef slopes,

T. derasa

is found predominantly in offshore coral reef areas, while

H. hippopus, H. porcellanus

and

T. squamosina

tend to prefer sandy areas, shallow lagoon flats and seagrass beds adjacent to coral reefs.

Available research on larval settlement preference offers some clues as to what may be driving the association with coral reefs. Several studies show that

T. squamosa

larvae prefer to settle on substrates of relatively high rugosity and are drawn to crustose coralline algae (CCA), but actively avoid settling on live coral (Courtois de Vicose, 2000; Calumpong

et al.,

2003; Neo

et al.,

2009). Additionally, the small giant clam (

T. maxima

) has shown an ability to discriminate between “favorable” and “unfavorable” habitats, preferring to settle near the effluent of conspecifics and near the effluent of live coral and CCA, rather than cyanobacteria and sponges (Dumas

et al.,

2014). However, this information is limited to only one of the seven species being analyzed in connection with this proposed rule, and there are no such data for species that are predominantly found in sand flats and seagrass beds, where rugosity is especially low and settlement cues might differ.

Based on the known features of giant clam biology and larval development, Lucas

et al.

(1989) hypothesized that the proximity of giant clams to coral reefs is, to some extent, a result of two environmental requirements, which are maximized in shallow reef habitats: (1) high light conditions to support the photosynthetic nutrition that giant clams derive from their algal symbionts, and (2) substrate rugosity to provide cryptic settlement locations for vulnerable recruits and juveniles. While we cannot conclude that these factors are equally important to all species of giant clams, it is within the context of these two habitat requirements that we discuss the following threats to coral reef ecosystems and their potential impacts to giant clams.

Climate Change Impacts to Coral Reefs

Reef-building corals typically occur in waters that range between 25 °C-30 °C and are highly sensitive to temperature excursions outside of this range (Brainard

et al.,

2011). Prolonged exposure to high temperature anomalies can lead to coral bleaching, where the coral host expels its symbiotic zooxanthellae, leaving the tissue translucent and revealing its white skeleton underneath. Bleaching-associated mortality is quite variable and can depend on the duration and intensity of elevated temperatures, geographic location, bleaching history, species present, and other factors (Pandolfi

et al.,

2011; Putnam & Edmunds, 2011; van Hooidonk & Huber, 2012). Mild to moderate bleaching does not always lead to death; however, repeated and prolonged bleaching can cause widespread coral mortality on regional or global scales. Extreme summer temperature anomalies associated with strong El Niño events have led to three recognized global bleaching events in 1997-98, 2009-10 and 2014-17 (Hughes, Kerry,

et al.,

2017; Lough

et al.,

2018; Eakin

et al.,

2019). The latest (2014-17) was the longest and most severe global bleaching event in recorded history. It affected every major coral reef region and led to the mortality of one third of the Great Barrier Reef in Australia (Couch

et al.,

2017; Hughes, Kerry,

et al.,

2017; Hughes, Kerry,

et al.,

2018). In addition, many other regional-scale bleaching events over the last several decades have caused widespread coral mortality in reef communities throughout the Indo-Pacific (Brainard

et al.,

2011; Hughes, Anderson,

et al.,

2018).

While coral bleaching patterns can be complex, there is a general consensus that rising global ocean temperatures have led to more frequent and severe coral bleaching and mortality events (Hughes, Anderson,

et al.,

2018; Lough

et al.,

2018). Without drastic action to curb greenhouse gas emissions, this trend is projected to continue throughout this century (van Hooidonk

et al.,

2016). Additionally, several studies have shown that warming can significantly increase coral susceptibility to disease (Bruno

et al.,

2007; Sokolow, 2009; Brainard

et al.,

2011; Howells

et al.,

2020). The combination of these warming-related impacts has already caused dramatic

declines in many coral species and changes to the composition and structure of coral reefs around the world (Brainard

et al.,

2011; Hughes, Barnes,

et al.,

2017; Hughes, Kerry,

et al.,

2018). During the major 2016 coral bleaching event on the Great Barrier Reef, for example, the fast-growing, structurally complex tabular and branching species suffered disproportionately (>75 percent mortality on heavily bleached reefs), shifting reef communities towards taxa with simpler morphological characteristics and slower growth rates (Hughes, Kerry,

et al.,

2018). Other studies similarly suggest that coral reef ecosystems, rather than disappear entirely as a result of warming, will likely persist, but with unpredictable changes to their community composition and ecological function (Pandolfi

et al.,

2011; Hughes

et al.,

2012).

Coral reefs are also facing increasing risk from ocean acidification, the process by which atmospheric carbon dioxide (CO

) is absorbed into the surface ocean, resulting in reduced seawater pH and reduced availability of carbonate ions. Due to anthropogenic CO

emissions, average surface ocean pH (total scale, pHt) has already decreased by more than 0.1 pHt units below the pre-industrial average of 8.17, and is expected to fall up to an additional 0.42 pHt units by 2100 under the worst-case emissions scenario from the Intergovernmental Panel on Climate Change (IPCC) (RCP 8.5) (Pörtner

et al.,

2014).

Such reductions in ocean pH could lead to drastic changes to the net calcification balance in many coral reef ecosystems. Numerous laboratory and mesocosm experiments have demonstrated a correlation between lower pH (or elevated partial pressure of CO

, pCO

) and decreased coral calcification rates (Anthony

et al.,

2008; Ries

et al.,

2009; Anthony

et al.,

2011; Gazeau

et al.,

2013; Albright

et al.,

2018). Brainard

et al.

(2011) provide a table summarizing the existing literature on the topic (table 3.2.2 of the report), and for every species studied, net calcification rate either declines, or in very few, there is no significant effect. In a pair of controlled mesocosm experiments, net community calcification of a small enclosed coral reef was found to increase under enhanced alkalinity and decrease after the addition of CO

(Albright

et al.,

2016; Albright

et al.,

2018), indicating that current levels of acidification are already impairing ecosystem-level calcification and will likely exacerbate this effect in the future. Coupled with dwindling coral cover due to warming-associated bleaching and mortality, continued acidification could transition many reef systems from net overall accretion to net erosion within this century (Eyre

et al.,

2018; Cornwall

et al.,

2021).

Others anticipate that ocean acidification will also weaken the structural integrity of coral reefs, both by promoting the efficiency of bioeroding organisms and by reducing reef cementation (

i.e.,

secondary processes of carbonate precipitation that bind the reef framework). Observations from coral reefs of the eastern Pacific, which occur in naturally low-pH upwelling zones reveal some of the highest rates of bioerosion documented globally, as well as poorly cemented, fragile, and unstable reef frameworks (Glynn, 1988; Eakin, 1996, 2001; Manzello

et al.,

2008). Crustose coralline algae (CCA) contribute significantly to reef cementation by consolidating loose rubble and sealing porous dead coral skeletons (Adey, 1998; Littler & Littler, 2013). There is major concern that CCA may be among the most sensitive taxa to declines in seawater pH, because they build their skeletons with magnesium-rich calcite, a highly soluble form of carbonate (Andersson

et al.,

2008). Although some argue that the risk to CCA may be over-estimated, as certain aspects of their skeletal structure and biology have proven resilient to projected future conditions (Nash

et al.,

2013; Nash

et al.,

2015; Nash

et al.,

2016). At this point, the potential impacts of ocean acidification on CCA are not fully resolved.

Given the documented and projected impacts of ocean warming and acidification on coral reef ecosystems, we assessed the direct implications of these impacts on the extinction risk of the seven giant clam species. In our previous status review for 82 species of corals, Brainard

et al.

(2011) concluded that “the combined direct and indirect effects of rising temperature, including increased incidence of disease, and ocean acidification [. . .] are likely to represent the greatest risks of extinction to all or most of the candidate coral species over the next century.” They assessed the threat of continued ocean warming to be “highly certain” and graded the threat as “high” for most regions where the candidate corals are known to occur. Based on this assessment, we find it likely that live coral cover in general will continue to decline due to more frequent and severe bleaching events, and that ecosystem-scale calcification rates will decline as a result. Critically for giant clams, the negative impacts of warming are most pronounced in the fast-growing branching and tabular coral species, which are the primary contributors to the three-dimensional complexity of reef habitats. Thus, continued loss of live coral cover and of these coral species in particular will likely severely reduce the rugosity of future reef ecosystems. There is also evidence that ocean acidification will further inhibit calcification rates of living corals and weaken the structural integrity of the reef framework, although the magnitude of these effects is not clear. As with ocean warming, the primary implication of these effects for giant clams will be reduced habitat rugosity.

Nevertheless, there are two important layers of uncertainty associated with these predictions, and especially their potential impacts to giant clam habitat. First, with respect to ocean acidification, carbonate chemistry is notoriously difficult to model precisely in open systems, as it relies on many physical and biological factors, including seawater temperature, proximity to land-based runoff and CO

seeps, proximity to sources of oceanic CO

, salinity, nutrients, as well as ecosystem-level photosynthesis and respiration rates. The last factor, in particular, means that in many cases, daily fluctuations in pH or carbonate chemistry can significantly outweigh projected long-term changes to the average (Manzello

et al.,

2012; Johnson

et al.,

2019). Secondly, as mentioned above, there is very little research establishing the degree to which giant clams rely on coral reef rugosity and thus might be impacted by any reduction thereof. The few larval choice experiments to date suggest that

T. squamosa

prefers rough to smooth surfaces and is attracted to CCA. However, most giant clam species can be found in an array of habitat types, and some even seem to prefer areas of low rugosity, such as sand flats and seagrass beds (

e.g., H. hippopus, H. porcellanus,

and

T. squamosina

). No studies have quantified how or if giant clams might be affected under varying levels of coral reef complexity.

If giant clams are sensitive to reductions in net ecosystem calcification and reef rugosity, the projected climate change-related impacts to coral reefs would likely pose a significant threat to

T. derasa, T. gigas, T. mbalavuana,

and

T. squamosa

within the foreseeable future, as these species are known to inhabit coral reef environments. We would expect decreased larval recruitment and juvenile survival across broad portions of their range. These early life stages are already known to suffer exceptionally

high mortality rates naturally, and any further reduction in productivity would greatly threaten the viability of remaining giant clam populations.

However, without more information on the direct association between substrate rugosity and giant clam survival and productivity, it is difficult to estimate with any confidence the degree to which reef rugosity must decline to threaten the persistence of these species. Likewise, given the lingering uncertainty in the dynamics and effects of ocean acidification, it is not possible to estimate a timespan over which such a risk can be expected. Thus, while it is likely that continued ocean warming and acidification will drastically alter coral reef communities and reduce the rugosity of many reef habitats, we concluded that the potential effect on the quality or suitability of giant clam habitat cannot be confidently assessed.

Coastal Development

The physical degradation of nearshore habitats due to coastal development poses an additional threat to giant clams throughout much of their range. Sedimentation associated with the construction and maintenance of coastal infrastructure can reduce the amount of suitable substrate available for larval settlement. There is extensive evidence for such an effect in corals—increased sediment load has been shown to deter larval recruitment (Babcock & Davies, 1991), reduce settlement success and survival (Hodgson, 1990; Babcock & Smith, 2002), and decrease the effectiveness of CCA to induce settlement (Ricardo

et al.,

2017). We could not find any research directly investigating this effect in giant clams; however, similarities in the biology and behavior of giant clam larvae would suggest that comparable results can reasonably be expected. Like coral larvae, giant clam larvae prefer rough settlement surfaces and are likely deterred by unconsolidated, fine-grained silt that is typical of anthropogenic sedimentation. Moreover, CCA provide a similarly important settlement cue for giant clams (Courtois de Vicose, 2000; Neo

et al.,

2009; Neo

et al.,

2015), and a reduction in effectiveness would likely decrease larval recruitment and settlement success.

Importantly, compared to habitat degradation due to climate change, coastal development poses a more localized threat to giant clam populations in specific regions. In the Red Sea, for example, Roa-Quiaoit (2005) notes intense modification to the Jordanian coastline over “four decades of rampant development of ports, industrial and tourism areas, as well as extreme events such as oil spills.” Surveys of giant clam density in the area revealed an inverse relationship between the population density of

T. squamosa

and metrics of human impact and coastal use. The author argues that the observed 12-fold reduction of giant clam density in Jordan over three decades is in major part due to this intense habitat modification. Similar examples of anthropogenic impacts to the coastal environment have also been documented in many areas of the Indo-Pacific region, although this is often discussed in relation to the health of coral reef ecosystems. In Singapore, approximately 60 percent coral reef area was lost during the 20th century due to land reclamation and associated sedimentation (Chou, 2006; Guest

et al.,

2008). On three specific Singapore reefs—Tanjong Teritip, Pulau Seringat, and Terumbu Bayan—Neo and Todd (2012) note that giant clams were once found, but the areas have since been reclaimed (covered over) in their entirety. In addition, more than 20 percent of coral reefs in Indonesia, 35 percent of reefs in Malaysia, 25 percent of reefs in Papua New Guinea, and 60 percent of reefs in the Philippines are threatened by the impacts of coastal development, including runoff from construction and waste from coastal communities (Burke

et al.,

2012).

In addition to undergoing intense coastal development activities over the past several decades, many of these areas are not well regulated with respect to coastal runoff and often do not prioritize sustainable management of the coastal environment (

e.g.,

Gladstone

et al.,

1999; O. A. Lee, 2010). In contrast, the Great Barrier Reef in Australia and island nations of the central and western Pacific, two other important areas of giant clam distribution, likely do not suffer the same effects of coastal development. Australia strictly enforces an integrated management plan to protect the Great Barrier Reef from the effects of coastal land use change via numerous national and State regulations, and the relatively small populations of most Pacific island nations minimize the impact of coastal development on surrounding waters.

Because

T. mbalavuana

and

T. derasa

reside preferentially in offshore coral reef areas, we conclude that habitat degradation of the nearshore environment related to coastal development likely does not pose a significant threat to these two species. With respect to

H. hippopus, T. gigas,

and

T. squamosa,

considering the relatively localized impacts of coastal development (

e.g.,

near heavily urbanized areas) compared to the size of the species' ranges, we conclude that the threat of habitat destruction, modification, or curtailment related to nearshore impacts of coastal development likely poses a low risk to

H. hippopus

and

T. gigas,

and a very low risk to

T. squamosa.

Specifically, we find the risk to be lower for

T. squamosa

due to the species' expansive geographic range as well as its current abundance and distribution, compared to

H. hippopus

and

T. gigas.

Because the restricted range of

H. porcellanus

is centered in a region of intense urban development (

i.e.,

within the densely populated Indo-Malay Archipelago), we conclude that habitat destruction and modification of the nearshore environment poses a moderate risk to the species. In other words, it likely contributes significantly to the species' long-term extinction risk, but given the localized nature of these impacts, does not in itself constitute a danger of extinction in the near future.

H. porcellanus

is also faced with an acute threat of habitat destruction in the northern portion of its range, where fishermen primarily from Tanmen, China have been razing shallow reef areas of the South China Sea in a search for giant clam shells (see

Tanmen Destructive Shell Harvesting

below). The damage from these operations is extensive and has likely eliminated any

H. porcellanus

that may have previously occurred in the islands of the South China Sea.

With respect to

T. squamosina,

we considered reports indicating specific areas of the Red Sea coastline which have been targeted for development of tourist activities and infrastructure, including Hurghada and the Gulf of Aqaba coastline from Sharm el-Sheikh to Nuweiba (Egypt), Eilat (Israel), and Aqaba (Jordan). These areas are significant, as they directly overlap with the majority of recent

T. squamosina

observations. As is mentioned above, Roa-Quiaoit (2005) estimated that 70 percent of the Jordanian coastline has been developed into ports, industrial centers, and tourism areas over the past several decades. Additionally, near Hurghada, Mekawy and Madkour (2012) observed dredging activities associated with a newly-constructed harbor and offshore trash disposal from boats. The authors also described industrial and tourist activities in several other areas along the coast of mainland Egypt (

e.g.,

oil drilling in El-Esh, dense industrial and tourism-related development near Safaga Harbor, high human activity in Quesir), which they argue have likely been the principal factors driving the

declining abundance of giant clams (primarily

T. maxima

) in these areas. Similarly, Hassan

et al.

(2002) reported “major decreases in giant clam populations between 1997 and 2002, with many small clams seen in 1997 not surviving through to 2002.” The authors attributed this population loss directly to sedimentation from major construction activities in South Sinai. While these studies address impacts to giant clams broadly, it is likely that

T. squamosina

experiences a similar threat in these areas. Lastly, Pappas

et al.

(2017) suggest that coastal development may, in combination with overutilization, explain the apparent absence of

T. squamosina

in the central Red Sea, but do not provide any data to support this claim.

Thus, while we do not have any data specifically linking habitat destruction, modification, or curtailment with the abundance of

T. squamosina,

based on the species' distribution in nearshore habitats, documented evidence of the impact of coastal development on giant clam abundance generally, and ongoing regional development goals, we conclude that this threat poses a high risk to

T. squamosina.

In other words, we find that it contributes significantly to the species' long-term extinction risk and is likely to contribute to its short-term extinction risk in the near future.

Tanmen Destructive Shell Harvesting

Despite a relatively small geographic scope, giant clam shell harvesting in the South China Sea has caused severe destruction of shallow water habitats. In the last decade, the small fishing village of Tanmen in China's Hainan province became a regional epicenter for giant clam shell handicraft and trade (Hongzhou, 2016; Larson, 2016; Lyons

et al.,

2018). From 2012 to 2015, the number of retailers of giant clam shell handicraft increased from 15 to more than 460, the number of shell carving workshops increased from a dozen to more than 100, and by the end of this period, it was estimated that this industry supported the livelihood of nearly 100,000 Tanmen residents (Hongzhou, 2016; Bale, 2017; Wildlife Justice Commission, 2021).

As the industry grew, many Tanmen fishermen increasingly abandoned the traditional fishing industry and shifted focus to giant clam shells as their primary livelihood. With local stocks of giant clams having been depleted by a long history of overharvesting, many fleets resorted to destructive methods of digging out large portions of coral reef using their boat propellers to access the shells of long-dead clams that had been buried under the reef substrate (Wildlife Justice Commission, 2021). As reported by V. R. Lee (2016), harvesting boats are anchored with a long rope or chain against which the propeller holds tension as it carves an arc-shaped scar in the reef (see also Wingfield-Hayes, 2015). The majority of this activity has occurred the South China Sea, and an analysis of satellite imagery revealed extensive damage in the Spratly Islands and Paracels, with an estimated 160 km

of coral reef in these areas completely destroyed by the combination of clam dredging and island-building activities (McManus, 2017).

In response to international pressures and following a 2016 arbitral tribunal ruling that China was aware of and responsible for “severe harm to the coral reef environment” in the South China Sea due in part to these activities (Permanent Court of Arbitration, 2016), steps were taken to halt destructive clam shell harvesting operations. China began to enforce anti-corruption measures aimed at undermining demand for the expensive jewelry and statues carved from giant clam shells (Bale, 2017), and in January 2017 the Hainan Province People's Congress passed new regulations that effectively banned the commercial trade of all giant clam species in Hainan (Wildlife Justice Commission, 2021). However, while giant clam shell harvesting operations were found to decline significantly between 2016 and 2018, the Wildlife Justice Commission (2021) reports several lines of evidence to suggest that “illegal giant clam shell trade persists in China in a covert manner with one clear supply area” (Hainan Province), and that a new influx of clam harvesting boats have returned since 2018. Thus, while the extensive damage to the habitat in this region would likely take several decades or more to undo if the ecosystems were allowed to recover, the ongoing threat of illegal harvesting is likely to prevent any substantial habitat recovery in the foreseeable future.

This threat of habitat loss is relevant to the species that are known to occur in this region and that are typically found in reef flat environments where the harvesting operations primarily occur. This includes

T. gigas, T. squamosa, H. hippopus,

and most critically

H. porcellanus,

which has a highly restricted range centered in the Sulawesi region of Indonesia but that extends northward into the Philippines and portions of the South China Sea (Wells, 1997; bin Othman

et al.,

2010; Neo

et al.,

2017). As is mentioned above, the damage from these operations has likely eliminated any

H. porcellanus

that may have previously occurred in the islands of the South China Sea.

Overutilization for Commercial, Recreational, Scientific, or Educational Purposes

The pervasive harvest of giant clams for subsistence and domestic sale, and several periods of short-lived but intensive commercial harvest have severely depleted giant clam populations throughout their respective ranges. Once the center of giant clam diversity in the region, the Philippines saw commercial exploitation of giant clams for the international shell trade decimate populations of

H. hippopus, H. porcellanus, T. gigas,

and

T. squamosa.

Similar trends have been observed throughout Southeast Asia (

i.e.,

Indonesia, Singapore, Thailand, Cambodia, Vietnam, and in the South China Sea), where each of these species except

T. squamosa

is now considered rare or locally extinct (Neo

et al.,

2017). Likewise, illegal harvest of giant clams for the international clam meat trade, primarily by Taiwanese fishermen or to supply Taiwanese demand, severely reduced giant clam populations throughout the western and central Pacific. As a result, as in Southeast Asia, nearly all of the species (excluding

T. squamosa

) are now considered rare or extinct throughout most of their Pacific range (Wells, 1997; Neo

et al.,

2017). Although international demand (primarily for the aquarium trade) is increasingly met by the growing field of giant clam mariculture, wild-sourced clams are still observed in international trade, and the potential for laundering wild clams with mariculture-produced specimens cannot be discounted (Sant, 1995).

Ongoing harvest for subsistence or domestic market supply, as well as persistent poaching, continues to limit substantial population recovery of giant clams throughout much of their range. As broadcast-spawning organisms with little to no mobility, giant clams are reliant on sufficient population density to facilitate gamete fertilization. Thus, even if small populations of giant clams have survived the years of exploitation, in many cases individuals may be too dispersed to successfully reproduce. Furthermore, the largest individuals were often targeted for the meat and shell trade, leading to altered size structures in remnant giant clam populations. Juveniles and smaller adults are known to be more susceptible to predators and to exhibit lower reproductive output, which will likely continue to limit population recovery in the near future. It is for these reasons that we consider overutilization to be the most significant threat to all seven giant clam species. Below, we

summarize the threats posed by overutilization related to subsistence fisheries, domestic markets, international trade, and illegal poaching, highlighting specific details related to each affected species.

Subsistence Fisheries

Giant clams have long been, and continue to be, an important component of traditional livelihoods and culture throughout their geographic range (Craig

et al.,

2011). As described by Lindsay

et al.

(2004), “there are few locations within the Pacific where tridacnids are not gathered on a daily basis and found in local markets” (Munro, 1993a). Archaeological evidence from shell middens (piles of discarded shells), which can be found across the Indo-Pacific from as far back as 2000 years ago (Swadling, 1977), as well as anecdotal accounts and local fishing practices all point to the importance of giant clam in Indo-Pacific diets (Neo & Loh, 2014). The shells of giant clams are also frequently carved for use as tools, containers, and ornaments (Copland & Lucas, 1988; Lucas, 1994).

Because

H. hippopus

is unattached to the substrate and occupies nearshore habitats that are relatively accessible to humans, it is an easy target for reef gleaners (

i.e.,

fishers that collect organisms by hand from nearshore sand and reef flats). Consequently, it has been a popular species for local harvest and consumption throughout its range. Many years of subsistence harvest have driven widespread population declines and local extirpations from many Pacific island nations and territories, including American Samoa, CNMI, and Guam.

In Fiji, for example, Seeto

et al.

(2012) discovered

H. hippopus

fossils in shell middens from two Lapita-era settlements (1100-550 B.C.), and found that shell size increased with midden depth, suggesting that human consumption contributed to population reductions and to its eventual extirpation. Surveys from Palau in the 1970s indicated that

H. hippopus

populations declined drastically as a direct result of overharvest (Bryan & McConnell, 1975). In Singapore,

H. hippopus

was considered rare historically (S. K. Lee, 1966; Dawson & Philipson, 1989), but consistent harvest pressure is thought to have prevented the species from establishing a sustainable population in the area and ultimately led to its extirpation (Neo & Todd, 2012). Additionally,

H. hippopus

continues to be exploited for consumption by coastal communities in Indonesia (Naguit

et al.,

2012), Malaysia (Neo & Todd, 2012), New Caledonia (Purcell

et al.,

2020), the Andaman and Nicobar Islands (Nandan

et al.,

2016), Papua New Guinea (Kinch, 2003), and virtually every other country where it occurs, except for Australia (Wells, 1997).

H. hippopus

has also been extirpated from American Samoa, CNMI, and Guam due to a long history of harvest for subsistence consumption and for sale in local markets (Munro and Heslinga, 1983; Sant, 1995; Wells, 1997; Green and Craig, 1999; Pinca

et al.,

2010). According to Score (2017), giant clams have a “special significance” in American Samoa culture and are often used as offerings during family and community gatherings when available. Moreover, Cunningham (1992) describes the cultural significance of giant clams to the Chamorro people, who live throughout the Mariana Islands, including CNMI and Guam. The common use of

H. hippopus

as a source of food and to make tools likely led to its extirpation in these locations (Wells, 1997).

Similar to

H. hippopus,

the tendency of

H. porcellanus

to occupy shallow nearshore areas make the species highly vulnerable to harvesting (Dolorosa

et al.,

2014). Heavy exploitation from both subsistence and commercial harvest has led to severe population declines throughout its range (Dolorosa

et al.,

2014; Neo

et al.,

2017). Villanoy

et al.

(1988) determined that

H. porcellanus

was overexploited in the Philippines as early as the 1980s, and more recently, Rubec

et al.

(2001) reported that

H. porcellanus

has been depleted to such an extent that it is no longer commercially viable for harvest in the Philippines. Ultimately, while subsistence harvest was widespread, heavy fishing pressure on giant clam stocks in the Philippines for the commercial shell trade has been the primary cause of population decline, and has led to local extinctions throughout the region (see International Trade in Giant Clam Shells and Shell-Craft below).

Because of their large size and fast growth rates,

T. derasa

and

T. gigas

have historically been two of the most widely exploited giant clam species for the consumption of their meat. Reports from throughout their ranges indicate that both species are harvested for subsistence consumption in nearly every location where they occur, with the major exception being the Great Barrier Reef and northwestern (NW) islands of Australia. There are certain Pacific island communities that attribute unique significance to

T. gigas

as a cultural symbol and place high value on the species as a food item for special occasions (Hviding, 1993). The shell of

T. gigas

is also valued as a traditional resource among many coastal communities for use as basins or as personal or religious decorations (Juinio

et al.,

1987; Hviding, 1993; Lucas, 1994). Both

T. derasa

and

T. gigas

are reported to have been extirpated from CNMI and Guam as a result of longstanding subsistence harvest (Wells, 1997; Pinca

et al.,

2010).

Based on the best available scientific and commercial data, it is likely that past and current subsistence harvest has played a significant role in the low abundance of

T. mbalavuana

throughout its range. S. Lee

et al.

(2018) attributes its absence from areas outside of the eastern Lau group in Fiji to a combination of ecological factors and “serial overfishing.” Additionally, Lewis and Ledua (1988) reported that in Fiji,

T. mbalavuana

is occasionally harvested unintentionally with

T. derasa,

due to the similarity in appearance between the two species. In Tonga,

T. mbalavuana

has traditionally been harvested for subsistence consumption and to supply domestic markets (Ledua

et al.,

1993), and although its occurrence in deeper areas may have offered some protection from harvest historically, the advancement of SCUBA and hookah gear has facilitated greater access to previously inaccessible stocks (Lewis & Ledua, 1988; Lucas

et al.,

1991; Neo

et al.,

2017). Interviews with a number of traditional fishermen indicated that the abundance of

T. mbalavuana

in Tonga had declined considerably during their lifetimes (Ledua

et al.,

1993). Harvest of giant clams for subsistence consumption and domestic markets is ongoing and largely unregulated in Fiji and Tonga.

Compared to the more common

T. maxima

and

T. crocea

(that are not themselves subject to this rulemaking), which often co-occur with

T. squamosa, T. squamosa

is typically larger and easier to physically remove from the reef, which makes it highly susceptible to harvest, particularly in shallow nearshore areas. For this reason,

T. squamosa

is an important resource in subsistence fisheries in nearly every location across its range, and in several locations, it is the preferred giant clam species for meat consumption (Neo

et al.,

2017). Few exceptions include Australia, where giant clam harvest is strictly prohibited, and remote areas where the distance from human settlements and infrastructure limits accessibility. However, in most locations where the species occurs, longstanding subsistence harvest has reportedly driven widespread population declines (Neo

et al.,

2017).

There are several studies that provide some insight as to the impact of past and current harvest on the abundance of the

T. squamosina

in the Red Sea. Paleolithic artifacts indicate that modern humans have been exploiting mollusks in the Red Sea for at least 125,000 years (Richter

et al.,

2008). During this time, Richter

et al.

(2008) found that giant clam communities in the Red Sea have changed dramatically from before the last interglacial period (122,000 to 125,000 years ago), when

T. squamosina

constituted approximately 80 percent of the shell remains, to

T. squamosina

comprising less than 5 percent of shells in freshly discarded shell middens. While the authors acknowledge that variable recruitment rates and mortality among the three Red Sea giant clam species may be attributed to natural disturbances, a concurrent decline in the size of giant clam shells strongly suggests that overutilization has played a significant role (Richter

et al.,

2008). In general, giant clam stocks in the Red Sea (including

T. maxima, T. squamosa,

and

T. squamosina

) have declined to less than 5 percent of their historical abundance in the 1980s and 1990s, largely due to artisanal reef-top gathering for meat and shells (Richter

et al.,

2008).

As with

H. hippopus

and

H. porcellanus,

the distribution of

T. squamosina

in shallow, nearshore habitats makes it particularly accessible to reef-top gatherers and exacerbates the threat of overutilization. Bodoy (1984) reported that giant clams had been subject to “heavy exploitation in the vicinity of Jeddah, Saudi Arabia, and they [were] often collected on the reef flat, both for food and for decorative purposes.” Additionally, two firsthand accounts from Gladstone (2000, 2002) described the harvest of “a significant number of clams” (primarily

T. maxima,

which is not subject to this rulemaking) from the Kharij As Sailah and Kharij Al Qabr areas of the Farasan Islands, noting that “clams were easily harvested in the shallow reef flats.” Overall, the best available scientific and commercial data suggest that giant clams have been harvested extensively in the Red Sea for many years, and given their traditional importance in the diets of coastal communities, harvest is likely ongoing in most areas of the Red Sea.

Domestic Markets (Meat and Shells)

In areas where giant clams were historically abundant, commercial fisheries often developed alongside subsistence harvesting to supply the local demand for giant clam meat and shells. In Fiji,

T. squamosa

and

T. derasa

were harvested by small-scale commercial operations and sold in 11 municipal markets or other direct sales outlets (Lewis

et al.,

1988). From 1979-1987, annual sale of giant clam meat in the domestic market ranged between 6 and 42 tons (Adams, 1988; Lewis

et al.,

1988; Wells, 1997). With respect to both species, Lewis

et al.

(1988) reported that the commercial harvest had driven once abundant populations to low densities, particularly near major urban centers.

Local markets also exist in a number of other Pacific countries and territories, although data on giant clam meat are often not reported at the species level. This is because of the difficulty in identifying the species once the meat is harvested since the shells are often left in the water, or because giant clam meat may have been mixed together or recorded collectively with other shellfish products when it was landed. Wells (1997) reported varying prices for giant clam meat from markets in American Samoa, the Solomon Islands (amounting to about 1 tonne of giant clam meat sold per year), the Marshall Islands (

H. hippopus

and

T. squamosa

), Niue, Vanuatu, Samoa, and FSM, where in 1990, 3.66 tonnes of giant clam meat were sold in the main markets of Chuuk. Data collected over a 10-week period in Tonga suggested that annual landings of giant clam meat for the domestic market might be 639-1,346 kg (Tacconi & Tisdell, 1992). Wells (1997) noted that in Jepara, Indonesia, giant clam meat was often sold dried, suggesting that the lack of fresh meat may be due to local overutilization of stocks. In Myanmar, clam meat was often marketed fresh for local consumption (Munro, 1989).

Additional reports indicate that domestic markets have continued in many of these localities into at least the early 2000s. In 1998-1999, nearly six tonnes of giant clam products were sold at a single market in Samoa (Skelton

et al.,

2000). Giant clam meat was still reported to be sold openly at markets in Malaysia as of 2003 (Shau-Hwai & Yasin, 2003). Until bag limits were established in 2009, the declared commercial catch of giant clams in New Caledonia varied between 1.5 and 9 tonnes per year. This included

T. derasa, T. squamosa,

and

H. hippopus,

and the authors indicate that it is often the adductor muscle that is sold in stalls of local markets. In the decade since the bag limits were put in place, commercial catch has fallen below 2 tonnes per year (Purcell

et al.,

2020). Kinch and Teitelbaum (2010) report that a high demand for giant clams to supply the local market in Tonga “has resulted in the over-exploitation of giant clam stocks in some areas.” In Papua New Guinea, Kinch (2003) attributes sparse populations of giant clams to commercial harvest, particularly that of Brooker Islanders. From January to September 1999, the author recorded the total sales of giant clam adductor muscle from Brooker Islanders to a local fishing company, which included 551 kg (or 1,970 clams) of specimens under 400 g and 146 kg (or 170 clams) greater than 400 g. Notably, nearly one-third of the

T. gigas

individuals included in these sales were not full-grown adults, which likely had an effect on the future productivity of those populations. Similarly, harvesting of giant clams for sale and subsistence use in Vanuatu has led to severely reduced populations that are “now considered close to collapse in many locations despite the presence of suitable habitats for juveniles and adults” (Dumas

et al.,

2012).

Domestic markets for giant clam shells are often related to the tourism industry. In the Andaman and Nicobar Islands of India, Nandan

et al.

(2016) report that giant clams, including

T. squamosa

and

H. hippopus,

are fished for the tourism-based ornamental shell industry. Additionally, in Thailand, giant clams shells are usually first sold to local traders in Phuket, and then sold to tourists as ornamental shells or various shell crafts (

e.g.,

ashtrays, soap trays, lamps) (Chantrapornsyl

et al.,

1996). Shells have also been a popular souvenir for tourists visiting beach and resort areas of the Philippines and Indonesia (Tisdell, 1994). At the Pangandarin and Pasir Putah beach resorts in Java, Indonesia, as many as 39 and 35 giant clam shells, respectively, were available for sale in 2013, despite a prohibition on the harvest and sale of giant clams (except under “exceptional circumstances”) under Indonesian law since 1987 (Nijman

et al.,

2015).

Prior to this prohibition, a major industry based on the use of giant clam shells for production of floor tiles (a.k.a, `teraso' tiles) led to the extensive harvest of giant clams in Indonesian waters. While much of the shell material was dead shells of

T. derasa

and

T. gigas

buried in reef flats, living specimens were known to be taken when found (Lucas, 1994). As described by Lucas (1994), there were tile production centers at Jakarta, Semarang, Bali, Manado, and likely Suabaya in the early 1980s, and clam shell trade routes had developed throughout the Indonesian islands to supply the industry. The best estimates of giant clam shell import to the Semarang tile production center from the nearby Karimun Jawa islands varied between about 20 and 200 tonnes per month over the period 1978-1983 (Brown & Muskanofola, 1985). At the

Jakarta production center, the clam shell trade was estimated to reach at least 600 tonnes per month in 1982 (Usher, 1984 cited in Lucas, 1994). This industry is no longer active in Indonesia as a result of the 1987 prohibition; however, it is likely that such intense demand contributed significantly to the depletion and current rarity of

T. derasa

and

T. gigas

in Indonesian waters and limited any potential for their recovery. Moreover, despite regulatory protection, all species of giant clams remain heavily exploited in Indonesia for their meat and shells, and some for the live aquarium trade (Neo

et al.,

2017). As a result of this overutilization, the larger giant clam species are now thought to occur in only a few locations archipelago-wide (Hernawan, 2010).

International Trade of Giant Clam Meat and Poaching

While giant clam meat is consumed throughout the Indo-Pacific region, Taiwan has consistently had the largest market and demand for giant clams. Some of the earliest references indicate that giant clams around Taiwan were depleted many decades ago (Pearson, 1977; Tisdell & Chen, 1994). As local stocks were rapidly exhausted, Taiwanese vessels began to range farther from their home ports, and from the 1960s to the mid-1980s, a surge of Taiwanese fishing vessels began illegally entering the waters of other Pacific nations in search of giant clam adductor muscle, particularly from the larger species,

T. gigas

and

T. derasa

(Munro, 1993a; Kinch & Teitelbaum, 2010). Occasionally, these vessels operated under agreements with local communities in exchange for resources (Adams, 1988), but in the vast majority of cases, giant clams were harvested illegally and to an unsustainable degree (Lucas, 1994; Kinch, 2002). The clam poachers progressively worked their way through the Pacific, typically concentrating their efforts on uninhabited islands and reefs where giant clam stocks had been virtually untouched and where local surveillance was limited. Reports of Taiwanese poaching include areas of the Philippines, FSM, Indonesia, Papua New Guinea, the Solomon Islands, Australia (the Great Barrier Reef), Palau, Fiji, Kiribati, and the Marshall Islands (Dawson & Philipson, 1989; Sant, 1995).

Data on the landings of giant clam meat in Taiwan are generally unavailable due both to their illegal nature and because in the records, landings were combined with meat of other marine molluscs and collectively referred to as `ganbei' or `compoy' (Lucas, 1994; Tisdell & Chen, 1994). Tisdell and Chen (1994) report that imports of ganbei ranged from 9 tons in 1977 to 621 tons in 1988. Other estimates of giant clam adductor muscle landings in the 1960s and 1970s range between 100 and 400 tons per year (Carlton, 1984; Dawson & Philipson, 1989). Dawson and Philipson (1989) estimated that during the peak of the Taiwanese fishery for giant clams, harvest did not likely exceed 100 tons of adductor muscle per year, though Munro (1989) regarded this to be an underestimate. Accounting for the potential harvest of the smaller species,

T. derasa

and

H. hippopus,

which have an adductor muscle about one-third the weight of

T. gigas,

those landings correspond to 300,000 to 450,000 clams per year. According to Dawson (1986), “it seems certain [. . .] that the total illegal harvest of giant clams over the twenty-odd years that such activities have occurred in the region can safely be measured in the millions.”

Poaching by long-range Taiwanese vessels peaked in the mid-1970s and gradually declined during the 1980s as the extension of exclusive economic zones, improved surveillance of reef areas, boat seizures, and depleted stocks made the fishery less profitable (Lucas, 1994). In addition, growing pressure from many Indo-Pacific nations forced the Taiwanese government to take stricter actions against giant clam harvesters (Dawson, 1986). The last five `compoy' (

i.e.,

clam and other shellfish) fishing licenses were rescinded by the Taiwanese government in 1982, mainly due to pressure from the Australian government, and beginning in 1986, the Taiwanese government began rejecting all requests for approval of Taiwanese involvement in any clam fishing activities, regardless of whether foreign agreement or license documents were provided. There is evidence, however, that some poaching activities continued in remote locations. From 1982 to 1987, at least four Taiwanese vessels were apprehended on outlying reefs of the Solomon Islands, in each case carrying clam meat from tens of thousands of giant clams (Govan

et al.,

1988). The authors note that the small size of the adductor muscles recovered indicates that large clams had likely already been harvested from the reef at an earlier date.

Even as Taiwanese poaching operations declined, the demand for giant clam meat in Taiwan persisted, incentivizing the development of legal commercial fisheries for export throughout the Indo-Pacific (Lewis

et al.,

1988; Basker, 1991; Lucas, 1994). It was estimated that imports of adductor muscle to Taiwan from these newly formed fisheries totaled approximately 30-40 tons in 1987 and 1988 (Tisdell & Chen, 1994). The fisheries, however, rapidly depleted local stocks and were in most cases short-lived, typically being shut down by local authorities in the span of a few years. In the Maldives, for example, commercial harvest of giant clams began in June 1990 and continued until early in 1991. Two buyers were operating and collectively harvested over 90,000 individuals; one buyer exported 9.8 tons to a Taiwanese buyer (Basker, 1991). Concerned over the high exploitation rate, the Ministry of Fisheries and Agriculture conducted an assessment of the giant clam stocks and fishery, and the resulting report recommended closing off high density areas to further fishing and other restrictions (Basker, 1991). The commercial fishery was subsequently closed, and collection of giant clams remains prohibited in the Maldives. Likewise, a commercial fishery in Papua New Guinea reportedly removed at least 85 tons of adductor muscle over a 5-year period, equivalent to over 750 tons total flesh weight, until it was closed due to depleted stocks (Munro, 1993a).

Adams (1988) described one example of the impact of extreme commercial harvesting pressure in Fiji when a ship named `Vaea' intensively harvested giant clam stocks in 1985. Teams of two harvesters on Hookah gear reportedly caught 50-250 clams per day. At one site, harvesters had taken approximately 80 percent of the standing stock of

T. derasa,

or nearly 15,000 individuals, from an area of 25.9 square miles down to a depth of 20 meters. Adams (1988) estimated that harvesting rates averaged 70 percent of the total living stock at each reef, less for scattered populations and more for denser ones. From 1984 to 1987,

T. derasa

catch rates in Fiji varied between 20 and 40 tons of flesh per year, half of which was exported (Adams, 1988). The Fijian fishery as a whole (including municipal markets, wholesale and retail outlets, and exports) landed over 149 tons during this period, with the largest annual harvest reaching 49.5 tons in 1984, the year in which exports began (Lewis

et al.,

1988).

By the early 1990s, pervasive stock depletions across the Indo-Pacific severely limited Taiwanese imports of giant clam meat (Tisdell and Chen, 1994). In the years since, many countries in the region have banned commercial export of giant clams, some have imposed size and/or bag limits, and many have become signatories to the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES). The regulatory

implications of CITES participation are discussed more thoroughly below in the section on

Inadequacy of Existing Regulatory Mechanisms,

but one of its requirements is that Parties must submit an annual report of their trade in CITES-listed species, including the number and type of permits and certificates granted, the countries involved, and the quantities and types of specimens traded. All species of giant clams have been listed under appendix II of CITES since 1985, and we can therefore rely to some extent on trade statistics from the CITES reporting database to characterize more recent patterns in the international market for giant clams.

In most cases, countries have limited their reporting to the family or genus level, and outside of a few instances of trade reported for

T. derasa, T. gigas,

and

T. squamosa,

no other species were identified specifically. Additionally, of all the transactions reported from 1983 to 2020, 50.4 percent and 39.5 percent were en route to New Zealand and the United States, respectively, while Japan, Singapore, and Australia comprised the remaining 10.1 percent of imports. Law Enforcement Management Information System (LEMIS) trade data provided by USFWS for the period 2016-2020 indicate that nearly all of the imports of giant clam meat over the past 5 years were classified to be of `Personal' nature, likely representing shipments intended for families or friends of Pacific islanders (Shang

et al.,

1994). Prior to 2000, there are several years in which countries reported significant export of meat from giant clams that had been born or bred in captivity. This includes 3615 kg and 472 kg of

T. gigas

and

T. derasa

meat, respectively, exported from Solomon Islands in the 1990s, 1695 kg of

T. derasa

meat exported from Palau in 1990-1991, and 65 kg of

T. gigas

meat exported from Australia.

A number of other countries have reported significant export of giant clam meat (species unknown) since the late 1990s, primarily to New Zealand and the United States. Nearly all of these exports are of wild-caught specimens, many of which have been seized or confiscated at the border due to improper or missing CITES export permits. The major exporters of giant clam meat in the last two decades include the Cook Islands, Kiribati, Marshall Islands, FSM, and Tonga. At the higher end, Tonga has exported an average of 1210 kg giant clam meat per year since 2005, and at the lower end, the FSM has averaged 58 kg per year during the same period.

Importantly, a number of the key countries in the trade of giant clam meat are not CITES contracting parties (

e.g.,

Cook Islands, Kiribati, Marshall Islands, FSM) or have only become so relatively recently (

e.g.,

Palau in 2004, Solomon Islands in 2007, Tonga in 2016). Thus, any trade reported for these countries is based on values reported by the CITES party involved, and any trade among two non-contracting nations is not included in these estimates. Additionally, the USFWS Office of Law Enforcement in Honolulu, Hawaii has reported that approximately 450 lbs (200 kg) of giant clam meat per year is refused (

i.e.,

seized, confiscated, or re-exported) from Tonga, FSM, and the Marshall Islands (K. Swindle, USFWS, pers. comm., December, 2017). This is likely a significant underestimate of the total amount of giant clam meat that comes into the United States (as a whole) illegally, as many shipments outside of those that pass through Honolulu likely make it past enforcement inadvertently (K. Swindle, USFWS, pers. comm., December, 2017). For these reasons, the CITES data should be viewed as incomplete, and the reported quantities are likely an underestimate of the total trade in giant clam meat.

International Trade in Giant Clam Shells and Shell-Craft

Giant clam shells have been used for a variety of decorative and utilitarian purposes, including as beads, vases, lamps, ashtrays, and wash basins.

H. hippopus

and

T. squamosa

are considered the most popular giant clam species for the shell trade (Shang

et al.,

1994) because of their unique physical characteristics (

e.g.,

attractive colors, bowl-like shape,

etc.

), although nearly all of the species have been harvested depending on the intended use, cultural preference, or geographic availability.

The Philippines has historically operated as the largest exporter of giant clam shells and shell-craft, accounting for over 95 percent of the global exports of giant clam shell products from 1983 to 2020. During the peak of the shell trade from 1979 to 1992, total exports from the Philippines surpassed 4.2 million kg (Juinio

et al.,

1987; Wells, 1997). While all species of giant clam that occur in the Philippines have been exploited, the two

Hippopus

spp. and

T. squamosa

were the most frequently used for ornamental purposes and handicrafts, and

T. gigas

was most frequently used for basins (Lucas, 1994). Juinio

et al.

(1987) noted that

T. derasa

may have also been harvested but was often not distinguished by shell dealers as a separate species; rather, it was known as a “heavier variety” of

T. gigas

H. porcellanus.

Export records from the Philippines Bureau of Fisheries and Aquatic Resources indicate an initial peak in 1979, when 1,003 tonnes of giant clam shells were exported, corresponding to 895,000 shell pairs. Exports then declined to a minimum of 63 tonnes (or 67,000 shell pairs) in 1982, which was thought to reflect saturation of the international demand. Juinio

et al.

(1987) reported that the demand for giant clam shells could be met from existing stock piles (except those of

H. porcellanus,

which was still considered to be highly marketable). However, exports began to increase again in the late 1980s and peaked in 1991 with nearly 1.2 million shells, over 460,000 carvings, and over 1,186 tonnes of shells (equivalent to about 825,000 shell pairs) exported in a single year (Wells, 1997). This occurred despite the government of the Philippines instituting a ban on the export of giant clams (except

T. crocea,

not subject to this rulemaking) in 1990. In the following year, exports declined to 374,000 shells and 70,000 carvings, likely due to the issuance of CITES Notification No. 663 (16 January 1992) urging all CITES Parties to refuse trade permits for Tridacninae products from the Philippines, in accordance with Philippine legislation (Wells, 1997). In the three decades since 1992, reported exports of giant clam shells from the Philippines have been considerably lower (but not absent), totaling only 8,528 shells and 6,359 carvings (CITES Trade Database, accessed 22 Mar 2022).

Ultimately, widespread subsistence harvest in conjunction with the heavy fishing pressure on giant clams to supply the commercial shell trade decimated the populations of several giant clam species (

e.g., H. hippopus, H. porcellanus, T. gigas,

and

T. squamosa

), with local extinctions widespread throughout the Philippines (Juinio

et al.,

1987). Wells (1997) reported that exports until 1992 were dominated by

H. hippopus, T. squamosa,

and

H. porcellanus,

with

H. hippopus

comprising 53 percent of shell exports and 94 percent of carvings. Even the few remaining locations thought to be the species' last strongholds in Philippine waters (

e.g.,

in the Sulu Archipelago and Southern Palawan) were overharvested by the mid-1980s (Villanoy

et al.,

1988). Presently, five of the seven giant species considered here (

H. hippopus, H. porcellanus, T. derasa, T. gigas,

and

T. squamosa

) can still be found in the Philippines and they are all protected by Philippine law. Native

T. gigas

populations are restricted to small portions of Tubbataha Reefs Natural Park in very low abundances;

T. derasa,

H. hippopus,

and

H. porcellanus

are considered rare, and

T. squamosa

is considered frequent (Neo

et al.,

2017).

The United States, Japan, Australia and various European countries have historically been the largest importers of shells and shell-craft from the Philippines (Juinio

et al.,

1987; Wells, 1997). The United States alone has accounted for over 50 percent of shells and over 60 percent of shell carvings imported between 1983 and 2020. More recently, however, dwindling giant clam populations as well as greater regulatory protections in many countries have limited the shell trade among the traditional major importers of the 1980s. Instead, the majority of international trade has shifted increasingly to illegal means. From 2016 to 2020, the global trade in giant clam shells based on CITES reports totaled 65,129 shells and 221 shells carvings (primarily

T. gigas

), of which over 92 percent originated in Indonesia and over 97 percent was imported by China. This has occurred despite a prohibition on the harvest and export of giant clams under Indonesian law since 1987. While not at the same scale as the Philippines, Indonesia has participated in the trade of giant clam shells and shell products since the 1980s. Once giant clams were listed as protected species in 1987, Tisdell (1992) suggested that unrecorded exports of giant clam shells continued to occur from Indonesia to the Philippines. Likewise, several reports in the years since indicate that enforcement of the harvest and export ban remains grossly insufficient and, as is suggested by the CITES reports, substantial export of giant clam shells from Indonesia is ongoing (Allen & McKenna, 2001; Nijman

et al.,

2015; Harahap

et al.,

2018).

Presently, the largest market for giant clam shells is in the city of Tanmen, in the southern Chinese Province of Hainan. As discussed previously, a major shell-crafting industry developed in this region during the 2000s. During the peak of the Tanmen shell-crafting industry in 2013-2014, there were an estimated 150 processing workshops supplying 900 craft shops with giant clam shell products in the province (Wildlife Justice Commission, 2021). The annual sales revenue of giant clam shell handicrafts in 2014 was estimated to be $75 million USD (Lyons

et al.,

2018). In January 2017, the Hainan Province People's Congress passed new regulations banning the commercial trade of giant clams in Hainan. However, investigations conducted 2 years later by the Wildlife Justice Commission (2021) found that there were still more than 100 craft shops in Tanmen, although fewer than 20 percent were still in business. Giant clam shell products were also being sold openly in hundreds of stores in other parts of the Hainan Province, such as Haikou, Sanya, Guangdong and Fujian provinces, and could be ordered on social media platforms, such as WeChat, for delivery to other locations (Wildlife Justice Commission, 2021). This has been corroborated by first-hand news reporting from Scarborough Shoal in April 2019, which documented ongoing shell harvesting by fishing boats flying the Chinese flag (ABS-CBN News, 2019). The ABS-CBN film crew captured many large piles of extracted giant clam shells around the harvesting area, some even extending above the water surface.

This industry primarily targets the shells of deceased clams embedded in the reef substrate; however, live clams are also taken whenever found. Large shells in particular are of the highest value, putting the remaining

T. gigas

populations in the area at the greatest risk. According to Lyons

et al.

(2018), “the more valuable [

T. gigas

] pieces come with a certificate of origin, specifying, for example, that it comes from Scarborough Shoal, Spratlys, or Paracels and, occasionally, even the specific reef concerned.” This suggests that

T. gigas

shells are considered to have different grades or qualities depending on where in the South China Sea they were harvested. As a result of this intense market demand in combination with the destructive shell harvesting methods described above, Gomez (2015) noted that

T. gigas

is now “virtually extinct” in the center of the South China Sea, including the Paracels, the Macclesfield Banks, and the Spratlys.

International Trade of Live Giant Clams for Aquaria

The largest current market for giant clams is that of live specimens for the aquarium trade and, to a lesser extent, to supply broodstock for mariculture operations. It can be difficult to distinguish the purpose of live specimen transactions from CITES reports alone, but Wells (1997) concluded “that the aquarium trade is now the main market for both wild-collected and mariculture clams.” In the 25 years since that report, the market for giant clams as aquarium specimens has continued to grow, with giant clams now representing one of the most desired groups of invertebrates in the aquarium industry (Wabnitz

et al.,

2003; Teitelbaum & Friedman, 2008; Mies, Dor,

et al.,

2017). They are a sought-after commodity and have been described as a “must have” item by collectors and aquarium hobbyists (Lindsay

et al.,

2004). The smaller, more brightly colored species (

i.e., T. maxima

and

T. crocea,

species not subject to this rulemaking) are by far the most popular in the marine ornamental trade, but

T. squamosa, T. gigas, T. derasa,

and

H. hippopus

are also traded in smaller numbers (Lindsay

et al.,

2004; Kinch & Teitelbaum, 2010).

CITES records indicate that the primary source countries for the seven species considered here include Australia, Palau, Vietnam, Solomon Islands, and Marshall Islands, among others. Notably, the vast majority of giant clams exported from Australia, Palau and Marshall Islands have been bred/born in captivity and thus pose less risk to wild populations; however, much of the export volume from Vietnam, Solomon Islands, Tonga, and more recently, Cambodia, are of wild-sourced specimens.

Of the seven species considered here,

T. derasa

and

T. squamosa

have been the most popular in the trade of live specimens, according to CITES reports. Comparing the two, exports of

T. derasa

have been higher from Pacific island nations, such as Palau, Solomon Islands, Marshall Islands, Tonga, and FSM. Nearly all recent trade of this species is of captive-bred/born individuals, with wild harvest in these countries contributing minimally, if at all, by 2010.

T. squamosa,

by comparison, has been harvested more often by countries in Southeast Asia, such as Vietnam, Cambodia and Indonesia, and many of the recent exports from Vietnam and Cambodia are of wild-sourced individuals. Exports from Vietnam peaked in the 2000s and have declined over the last decade, while exports from Cambodia have increased more recently, reaching nearly 10,000

T. squamosa

specimens in 2019. Neo

et al.

(2017) notes that the decline in exports from Vietnam is related to trade restrictions implemented in response to concerns and regulations sourcing wild specimens, and it is possible that some giant clams from Vietnam have been re-routed for export through Cambodia. In fact, according to CITES reports, over 99 percent of the recorded

T. squamosa

exports from Cambodia were imported by Vietnam, implying a close trade connection between the two nations. Neither

H. hippopus

nor

T. gigas

have been harvested consistently for the aquarium trade, although with respect to

T. gigas,

Craig

et al.

(2011) attributed this to a lack of available supply rather than a decline in demand. Because of declining populations throughout much of its range, the majority

T. gigas

specimens for the aquarium trade in the late 2000s were being sourced from just a few small island nations, primarily Tonga (Craig

et al.,

2011). However, according to CITES records, trade of

T. gigas

from Tonga has not occurred since 2011.

T. gigas

is not considered to be native to Tonga, but had reportedly been introduced there as part of stock enhancement and aquaculture programs (Munro, 1993a; Wells, 1997). According to a CITES assessment in 2004, the introduced populations of

T. gigas

had by that point died out, so it is not clear where the exported specimens originated (CITES, 2004a).

The United States has consistently been one of the top import markets for live giant clams, along with Canada, several countries in Europe, Japan and Hong Kong (Wabnitz

et al.,

2003; Craig

et al.,

2011). In 2002, 70 percent of the giant clams exported for the aquarium trade went to the United States (Mingoa-Licuanan & Gomez, 2002 cited in Craig

et al.,

2011). According to CITES reports from 1983-2020, the United States has accounted for 24.2 percent of the total recorded imports of

H. hippopus,

53 percent of imports of

T. derasa,

56 percent of imports of

T. gigas,

38.4 percent of imports of

T. squamosa,

and 12.8 percent of imports of Tridacninae specimens that were not identified to the species level. Throughout the full record since 1983, 50.6 percent of the imports to the United States were recorded as captive-bred/born specimens, while 44.7 percent were recorded as wild-sourced; however, according to LEMIS data for the period 2016-2020, wild-sourced specimens now represent only 4 percent of imports, with captive-bred/born specimens accounting for the remaining 96 percent.

Summary of Risks to Specific Species Due to Overutilization for Commercial Purposes

After considering the best available scientific and commercial data presented above and in the Status Review Report, we reached several different conclusions regarding the threat of overutilization for various commercial purposes to the seven giant clam species considered here. We summarize these conclusions of the risks for this threat category for each species below.

H. hippopus

A long history of subsistence harvest punctuated by two decades of intense commercial exploitation for the shell and shell-craft industry have led to severe declines of

H. hippopus

populations throughout its range. As is mentioned above,

H. hippopus

has been one of the most popular giant clam species in the international shell trade because of its size and physical characteristics (

e.g.,

attractive colors, bowl-like shape) (Shang

et al.,

1994). The Philippines operated as the largest exporter of giant clam shells in the 1970s and 1980s, with

H. hippopus

being the most frequently traded species during this time. According to CITES annual report data, over 277,000 kg, 341,000 shell pairs, 2 million “shells” (without associated units), and 1.7 million shell carvings of

H. hippopus

were exported from the Philippines from 1985 to 1993. This period of intense harvest left

H. hippopus

severely depleted throughout the Philippines and much of Southeast Asia, where it remains at very low abundance except in a few isolated areas.

While most countries have imposed prohibitions on the commercial exploitation of giant clams and CITES records indicate that recent international trade of

H. hippopus

is minimal, subsistence harvest continues to pose a threat to the species in most populated areas where it occurs. Without more thorough monitoring from many of these locations, it is difficult to determine if this ongoing harvest is causing further population declines, but at the very least, it is likely preventing any substantial rebound of depleted populations throughout its range. An important exception is Australia, where anecdotal reports suggest that strictly enforced harvest bans have been largely successful in preventing overutilization and protecting reportedly healthy stocks of this species. For these reasons, and considering the documented effects of past harvest for the international shell trade on species abundance, we conclude that overutilization of

H. hippopus

contributes significantly to the species' long-term risk of extinction.

H. porcellanus

As is mentioned above, heavy fishing pressure on

H. porcellanus

in the Philippines for the commercial shell trade has been the primary cause of population decline, and has led to local extinction of the species throughout the region (Juinio

et al.,

1987). Villanoy

et al.

(1988) documented the export volume of giant clam shells from one major shell dealer in the Zamboanga region of the Philippines, San Luis Shell Industries. From 1978 to 1985, approximately 413,230 pairs of shells were exported by this company, of which about 37 percent (or nearly 153,000) were

H. porcellanus.

Based on comparisons to data provided by Juinio

et al.

(1987), the authors estimate that this shell dealer accounted for approximately 18.5 percent of the estimated total export volume of giant clam shells from the Zamboanga region during this period, suggesting that the total harvest of

H. porcellanus

during this period was likely much higher. According to CITES annual reports, from 1985 to 1992, the Philippines exported an additional 576,298

H. porcellanus

shells, 145,926 shell pairs, 179,043.5 kg of shell material, 293,110 shell carvings, and 38,138 kg of shell carvings. All were either reported to be wild-caught or did not include the source of harvest. No other nation reported export volumes close to this magnitude during this time. Malaysia reported the export of 500 kg of shell material in 1985, and Indonesia reported the export of 100 kg of shell material in 1986, but there are no other CITES reports relating to

H. porcellanus

from these two countries. CITES reports also indicate that 16

H. porcellanus

were exported as live specimens from the Philippines to Norway and Germany in 1992 and 1997, respectively; there have been no exports of live

H. porcellanus

specimens since. Additionally, export of 35 live specimens from the Solomon Islands to Germany and the United States was reported in 1997, but this is likely a reporting error, as this species has not been observed in the Solomon Islands.

In Indonesia,

H. porcellanus

is extremely rare. It was historically, and still is reportedly, exploited for its meat and shells when it is found (Pasaribu, 1988; Neo

et al.,

2017). Consequently, the species is now thought to occur in only a few locations in Indonesia (Hernawan, 2010; Wakum

et al.,

2017). Likewise,

H. porcellanus

abundance is also declining in Malaysia, in part due to ongoing harvest of meat and shells (Neo

et al.,

2017). As they are considered rare and are restricted to Sabah and Pulau Bidong on the east coast of Peninsular Malaysia, continued harvest likely threatens the persistence of these populations. Additionally, international poaching continues to pose a threat, as authorities from both Malaysia and the Philippines reported an increase in the number of fishing boats illegally harvesting giant clams as recently as 2010-2015 (Neo

et al.,

2017).

Overall, it is clear that intense historical commercial demand for

H. porcellanus

led to severe population declines and the current low abundance of the species throughout its range. Furthermore, ongoing subsistence harvest and poaching of giant clams throughout the South Asia region continue to threaten the few

populations of

H. porcellanus

that remain. Accordingly, we conclude that overutilization is contributing significantly to the long-term extinction risk of

H. porcellanus

and is likely to contribute to short-term extinction risk in the near future.

T. derasa and T. gigas

Due to the similarities of the threat to

T. derasa

and

T. gigas,

we present the conclusions for these two species together. Overall, the best available scientific and commercial data indicate that both

T. derasa

and

T. gigas

have been widely exploited for many years for their meat, shells, and as popular aquarium specimens. Many consider

T. gigas

to be the most heavily exploited among all giant clams (Craig

et al.,

2011; Mies, Scozzafave,

et al.,

2017; Neo

et al.,

2017), noting its extensive harvest for its meat and shells in nearly every location where it has occurred. Similarly,

T. derasa

is also highly valued as a food source throughout the entirety of its range. For over two decades, both species were subject to an intense commercial demand for the meat of their adductor muscle, primarily from consumers in Taiwan. Widespread harvest and poaching to supply this commercial market caused severe, documented population losses throughout the majority of the species' ranges. The commercial demand for giant clam meat began to decline by the end of the 1980s due to the low abundance of remaining populations in conjunction with stricter harvest regulations and improved enforcement. However, due to their traditional importance as a food source in many cultures, subsistence harvest of

T. derasa

and

T. gigas

continues in most locations throughout their respective ranges, which may lead to further population decline and likely prevents any substantial recovery of depleted populations.

Furthermore, recent CITES records and available reports indicate that

T. gigas

shells continue to be traded in high volumes from Indonesia to China despite a prohibition on the harvest and export of giant clams that has been in place under Indonesian law since 1987 (Allen & McKenna, 2001; Nijman

et al.,

2015; Harahap

et al.,

2018).

The Great Barrier Reef and outlying islands of NW Australia are, for the most part, an exception to the range-wide trends for these species. Northern areas of the Great Barrier Reef were subjected to widespread poaching of

T. derasa

and

T. gigas

in the 1970s and 1980s, but improved surveillance of Australian fishing grounds and stronger enforcement of harvest bans reduced the poaching pressure considerably. As a result, harvest of the two species in Australian waters since the 1980s has likely been minimal. Recent quantitative estimates of abundance are scarce, but based on past surveys and the strong protective measures in place, most experts consider the Great Barrier Reef to have relatively large, stable populations of giant clams, including

T. derasa

and

T. gigas

(Neo

et al.,

2017; Wells, 1997).

Overall, we consider the severe impact of past harvest on species abundance range-wide alongside reports of ongoing subsistence and commercial use in most locations except Australia. Based on this information, we conclude that overutilization of

T. derasa

and

T. gigas

contributes significantly to the species' long-term extinction risk. However, because the threat is minimal in Australia, which represents a substantial proportion of suitable habitat within these species' respective ranges, and where populations are reportedly healthy, this factor likely does not constitute a danger of extinction to the two species in the near future.

T. mbalavuana

As is discussed above, harvest of giant clams for subsistence consumption and domestic markets is ongoing and largely unregulated in Fiji and Tonga. Thus, given the highly restricted range and general scarcity of

T. mbalavuana,

we conclude that the threat of overutilization for commercial purposes contributes significantly to the species' long-term extinction risk and is likely to contribute to the short-term risk of extinction in the near future.

T. squamosa

has been harvested extensively for both subsistence and commercial purposes for several decades, which has led to documented population declines in many areas of its range (Neo

et al.,

2017). While most countries have imposed prohibitions on the commercial exploitation of giant clams, the demand for

T. squamosa

in the ornamental aquarium market continues to pose a threat to wild populations in Cambodia and Vietnam. Additionally, subsistence harvest is ongoing in most populated areas where the species occurs. Without more thorough monitoring from many of these locations, it is difficult to determine if this ongoing harvest is causing further population declines, but at the very least, it is likely preventing any substantial rebound of depleted populations throughout its range. As with other species, an important exception is Australia, where anecdotal reports suggest that strictly enforced harvest bans have been largely successful in preventing overutilization and protecting reportedly healthy stocks of giant clams. For these reasons, and considering the documented effects of past harvest on species abundance, we conclude that overutilization of

T. squamosa

contributes significantly to the species' long-term risk of extinction, but does not in itself constitute a danger of extinction in the near future.

T. squamosina

The best available scientific and commercial data suggest that giant clams (including

T. squamosina

) have been harvested extensively in the Red Sea for many years. Given their traditional importance in the diets of coastal communities, harvest is likely ongoing in most areas of the Red Sea. In combination with the natural accessibility of

T. squamosina

in shallow nearshore areas, this past and ongoing harvest pressure has likely contributed significantly to the exceptionally low abundance of this species throughout the region. We are aware of 30 documented observations of

T. squamosina

since its re-discovery in 2008. This includes 17 specimens from the Gulf of Aqaba and northern Red Sea (Roa-Quiaoit, 2005; Richter

et al.,

2008; Huber & Eschner, 2011; Fauvelot

et al.,

2020), seven individuals from the Farasan Islands in southern Saudi Arabia (Fauvelot

et al.,

2020; K.K. Lim

et al.,

2021), and six individuals from an unnamed site in the southern Red Sea (Rossbach

et al.,

2021). As an indication of its exceptionally low abundance at present, Rossbach

et al.

(2021) surveyed 58 sites along the entire eastern coast of the Red Sea, from the Gulf of Aqaba down to southern Saudi Arabia, and observed six

T. squamosina

at only one survey site in the southern Red Sea. Similarly, Pappas

et al.

(2017) did not encounter any

T. squamosina

at nine survey sites in the central Red Sea. With so few

T. squamosina

remaining, we conclude that this factor is likely to contribute to short-term extinction risk in the near future.

Disease or Predation

There are a number of infectious diseases and parasites that have been reported in giant clams, most often either bacterial or protozoan in origin (Braley, 1992; Mies, Scozzafave,

et al.,

2017). Bacterial infections are most often caused by

Rickettsia

sp., which infect the ctenidia (gill-like respiratory organ) and the digestive lining of the clam (Norton

et al.,

1993; Mies, Scozzafave,

et al.,

2017). Protozoan

infections are often caused by either

Marteilia

sp. or

Perkinsus

spp. Giant clams with

Marteilia

infections show no external symptoms, but the infection will eventually cause superficial lesions on the kidney (Mies, Scozzafave,

et al.,

2017).

Perkinosis, also known as pinched mantle syndrome, is caused by

Perkinsus

spp. Giant clams typically do not exhibit any symptoms of the infection until they become immunosuppressed due to some other environmental stress. At that point, the protozoan population is able to proliferate, and in some cases causes mortality of the host clam. Once the clam dies, trophozoites of

Perkinsus

spp. become waterborne and can infect nearby individuals (Mies, Scozzafave,

et al.,

2017). A significant rate of infection by

Perkinsus

spp. was previously observed at several sites on the Great Barrier Reef, with 38 of 104 sampled individuals (including

T. gigas

and

H. hippopus

) being infected (Goggin & Lester, 1987). Additionally, several

Perkinsus

infections were observed in association with a mass mortality of giant clams at Lizard Island in Australia in 1985; however, the cause of the death was never determined and the infections may have been coincidental (Alder & Braley, 1989).

Giant clams are also affected by external parasites, including snails, sponges, and algae. Pyramidellid snails are particularly invasive, exploiting the clams by inserting their proboscises (

i.e.,

feeding appendage) into the clam tissue and consuming the hemolymph within the siphonal mantle (Braley, 1992). On rare occasions, the snails may prove fatal to juvenile clams, but they are unlikely to cause mortality in adult clams (Mies, Scozzafave,

et al.,

2017). Other external parasites (

i.e.,

sponges and algae) are typically more of a nuisance to giant clams rather than fatal infestations. For instance, boring sponges (

e.g., Cliona)

may drill holes into the clam's shells, and algae (

e.g., Gracilaria

sp.) may overcrowd the shell and prevent the mantle from extending, but neither of these parasites typically cause mortality (Mies, Scozzafave,

et al.,

2017).

When disease is present, giant clams exhibit physical symptoms that are usually quite obvious, including a retracted mantle (typically the initial symptom), a gaping incurrent siphon (indicative of more advanced disease), and discarding of the byssal gland (Mies, Scozzafave,

et al.,

2017). While some diseases may respond to antibiotics, concentrations and dosages for giant clams have not been well studied. Overall, the prevalence and severity of disease likely vary across the extensive range of giant clams, but there is no information to indicate that disease is an operative threat to giant clams to the extent that it is significantly increasing the extinction risk of the species addressed here.

Much of what is known regarding predation of giant clams has been learned from the ocean nursery phase of mariculture activities, when juveniles are outplanted to their natural environment (Govan, 1992). Giant clams are widely exploited as a food source on coral reefs, with 75 known predators that employ a variety of attack methods (see table 3 in Neo, Eckman,

et al.

(2015) for a comprehensive list). These predators are largely benthic organisms, including balistid fishes, octopods, xanthid crabs, and muricid gastropods (Govan, 1992). The fishes (

e.g.,

wrasse, triggerfish, and pufferfish) prey on both juvenile and adult giant clams by biting the mantle edge, the exposed byssus, or extended foot. Other predators (

e.g.,

crabs, snails, and mantis shrimp) have been observed chipping, drilling holes into, and/or crushing the shells of smaller individuals (see review in Neo

et al.

2015). Heslinga

et al.

(1984) observed several instances of predation firsthand in association with giant clam culturing operations in Palau. Large muricid snails (

Chicoreus ramosus

) were found to attack, kill, and eat

T. squamosa

specimens up to at least 300 mm shell length, and a single hermit crab was able to crush 26

T. gigas

juveniles (20-30 mm) when inadvertently left in the culture tank. The authors also noted circumstantial evidence of predation by

Octopus

spp. in Palau based on the characteristically chipped shells of giant clams often observed outside of octopus dens.

Giant clams employ a suite of defense mechanisms, both morphological and behavioral, to resist predatory attacks (Soo & Todd, 2014). For example, their large body size, small byssal orifice, and strong shells create physical barriers to predation. In addition,

T. squamosa

is equipped with hard, scaly projections on its shell known as scutes that have been shown to provide protection from crushing predators (Han

et al.,

2008). Giant clams also exhibit behavioral defense mechanisms, such as aggregation, camouflage, rapid mantle withdrawal (Todd

et al.,

2009) and squirting water from siphons (Neo & Todd, 2010). While the ability of giant clams to endure intense predation pressure and acclimate to repeated disturbance can have implications

This text is long and has been trimmed here. Open the source document for the complete record.

This is a copy of a public record, reproduced as it was published. It is not legal advice, and it may not be the version a court would rely on. Check the official source before you cite it.