Introduction
Conservation status assessments, conservation priority setting, and decisions about whether a species will receive special protections under state and federal laws rely upon foundational survey data (Jones et al.
2013; Smith et al.
2018). Survey data are also critical to understanding historical trends and, in the most extreme case, for declaring a species extinct. However, poorly-designed surveys and monitoring programs can cause more harm than good (Yoccoz et al.
2001; Lindenmayer and Likens
2009). For example, inadequate surveys could lead a governmental agency to prematurely declare a species extinct, which would then cause a species in need of conservation to be overlooked. Although recommendations for effective monitoring exist, they rely on conservation practitioners being able to make informed study designs suitable for the taxon or ecosystem of interest (Lindenmayer and Likens
2009). Data to inform such study designs are often lacking for understudied invertebrates, which are usually those most in need of conservation attention (Johnson et al.
2013; Haag and Williams
2014). Thus, information is required for understudied taxa about whether the best approach for surveys will be those that emphasize sampling as many sites as possible or those that emphasize expending a high sampling effort at a small number of sites. For species that have been rediscovered after being considered extinct, understanding why and how surveys failed to detect those species should also ensure better overall status assessments. Moreover, to influence policy makers, conservation-related success stories are needed to emphasize the real-world benefits of well-designed surveys for understudied taxa.
Freshwater gastropods are among the most imperiled taxa in the world, but they are also among the least researched (Johnson et al.
2013; Böhm et al.
2021). Freshwater gastropods persist ubiquitously throughout a variety of aquatic habitats and drive ecosystem function by playing a pivotal role in aquatic food webs and nutrient cycling (Strong et al.
2008; Atkinson et al.
2023). The southeastern United States is a hotspot of freshwater gastropod biodiversity where many species are restricted to single drainages or isolated within small springs (Lydeard and Mayden
1995; Johnson et al.
2013). In the last 35 years, at least eight freshwater gastropods that were once considered extinct have been rediscovered (e.g., Adams and Gerberich
1988; Hershler et al.
1990; Minton et al.
2003; Ó Foighil et al.
2011; Whelan et al.
2012; and see Johnson et al.
2013; Whelan et al.
2022). However, past research has been equivocal as to why those species were overlooked to the point of being declared extinct. For example, one reason a species could be prematurely declared extinct is that no reasonable amount of survey work would have allowed for past detection if a given species underwent drastic, below detection limit population size declines across its range and then expanded in response to habitat improvements. Another reason would be that survey work was inadequate if a species persisted at some locations that were simply not surveyed prior to an extinction declaration. Determining why an understudied species was overlooked should reveal whether premature declaration of extinctions can be avoided.
No other freshwater gastropod family has seen as many putative extinctions as Pleuroceridae (Johnson et al.
2013; IUCN
2022). In the most extreme instance, the entire genus
Gyrotoma went extinct after numerous impoundments were installed on the Coosa River in Alabama, USA during the 20th century (Bogan and Pierson
1993). However, recent work offers encouraging results for pleurocerids, including the rediscovery of the narrow-range endemic
Leptoxis compacta (Whelan et al.
2012). Furthermore, some species were recently determined to be more widespread than previously thought (e.g.,
Leptoxis ampla and
Pleurocera foremani) (Whelan et al.
2019; Redak et al.
2021). Yet, a question remains as to why these species and populations were overlooked for many years.
Here, we describe survey work that resulted in rediscovering
Lithasia hubrichti, a species thought to be extinct for nearly 60 years (Hartfield
1993; Johnson et al.
2013). In doing so, we examine the real-world benefits of improved surveys for freshwater gastropods.
Lithasia hubrichti had not been seen since its description in 1965, and the species was previously known from only one location in Mississippi, USA (Table
S1; Clench
1965; Hartfield
1993). However, the aforementioned discoveries of putatively extinct or extirpated pleurocerids motivated us to look for
L. hubrichti. We compared the conchological and radular morphology of collected specimens with historical museum material to ensure that putative
L. hubrichti individuals were not another species. We also generated genomic data to model demographic history of the species, which can provide insights as to whether
L. hubrichti was overlooked as result of low abundance at some point since its description or if it was overlooked because it persisted within an unsurveyed stretch of river. This study also explains why other rediscovered freshwater gastropods were overlooked in the recent past and should influence future status assessments of understudied invertebrates.
Discussion
We rediscovered
Lithasia hubrichti after it was overlooked for nearly 60 years, Despite being considered extinct, population genomic data indicated that
L. hubrichti has persisted at high abundance in some stretches of the Big Black River before and since the species was formally described. Thus, the species was overlooked because not enough sites were surveyed, not because the species had suffered a range-wide decrease in abundance. Rapid surveys, like the ones done here, also led to previous gastropod rediscoveries (Ó Foighil et al.
2011; Whelan et al.
2012) or discovery of larger ranges (Whelan et al.
2019; Redak et al.
2021). Since the description of
L. hubrichti there have been multiple attempts to detect the species at its type locality by United States Fish and Wildlife Service and other researchers (P. Hartfield,
pers. observation; F. Thompson,
pers. communication; L. Hubricht,
pers. communication), but because the species distribution also coincides with a publicly-inaccessible reach of the river, seldom effort was made to find the species at novel localities. Furthermore, low water conditions may have been important in the rediscovery of
L. hubrichti due to the naturally-high turbidity levels within the Big Black River at base flow. Thus, our results and those of past studies clearly demonstrate that sampling as many sites as possible under low water levels, rather than expending high sampling effort at one or a few sites, is the best strategy for uncovering overlooked populations of understudied gastropods. That is, sampling more sites will give the best odds at encountering habitats where narrow-range endemics persist. In contrast, sampling a small number of sites (e.g., those at road crossings or only the type locality) with a high amount of effort or when sampling conditions are not ideal (e.g., high water levels) can result in failing to capture any given species and result in premature extinction declarations.
Our conclusions about the need to sample as many sites as possible to understand whether a species is still extant and to understand the range of imperiled species likely hold across Pleuroceridae and other freshwater gastropod families. As with
L. hubrichti, other recent rediscoveries of freshwater gastropods in multiple families have occurred at locations where the putatively extinct species was locally abundant and easily sampled in a short time frame (Hershler et al.
1990; Ó Foighil et al.
2011; Whelan et al.
2012; Johnson et al.
2013). These rediscoveries resulted from increased freshwater mollusk surveys that emphasized unsampled, often hard to reach, sites. The ease of finding the species from the above examples, once the appropriate site was surveyed, supports the notion that our case study on
Lithasia hubrichti is widely applicable.
To the best of our knowledge, demographic modeling has not been done on any other freshwater gastropod that was once thought to be extinct. However, genetic diversity estimates that were previously reported for another species that was once considered extinct,
Leptoxis compacta, are also not consistent with what is expected after a bottleneck (Wright et al.
2020). Furthermore, no study has presented data that would indicate that previously-rediscovered gastropods were overlooked because they underwent a severe bottleneck followed by population expansion that facilitated their rediscovery. Therefore, genomic data examined here and from previous studies support our hypothesis that rediscovered species were overlooked because not enough sites were sampled, not because of a lack of survey effort at sampled sites. Thus, if tradeoffs between site number and survey effort per site are needed because of limited resources, our findings, and those of others, support policies and practices that favor sampling as many sites as possible to assess conservation status. Such surveys are particularly necessary before a species is declared extinct. Surveys that emphasize a higher number of sites over more time spent at any given site will also fill in gaps of our understanding of contemporary ranges for any under-surveyed species.
Policies and practice that emphasize surveys with many sites will also need to be coupled with policies that encourage collaborative relationships between landowners and conservation practitioners. However, positive engagement with landowners can be difficult, at least in some countries like the United States. For example, in the United States, Brook et al. (
2003) found that over 50% of landowners in the range of the endangered Preble’s Meadow Jumping Mouse either refused, or would refuse, to allow biologists to perform surveys on their land. In the case of
L. hubrichti, sampling at the rediscovery site during low enough flow would have been extremely difficult (i.e., at least a 2 + hour jet boat ride over shallow shoals), or impossible, without having been granted access to field sites by local private landowners. Without access through their property,
L. hubrichti may still be considered extinct.
Our results also emphasize the benefits of considering multiple taxonomic groups when performing surveys. The discovery of one dead L. hubrichti shell was the impetus for our overall finding, but the shell was sampled during drainage-wide survey work focusing on freshwater mussels. Had the shell been discarded as a non-target taxon, L. hubrichti would likely still be considered extinct. Similarly, the case of L. hubrichti emphasizes the need for taxonomic expertise, which is limited for freshwater gastropods and other invertebrate groups. Without type comparisons and morphological comparisons of radulae, the identity of the snails collected in the Big Black River would be much more uncertain. Such uncertainty could have dissuaded agencies from pursuing conservation of L. hubrichti. We are certainly not the first to emphasize the importance of taxonomy in surveys and conservation, and we hope that this case study will aid in stimulating policies that encourage and fund taxonomic expertise and research.
Conservation status and recommendations for Lithasia hubrichti.
Prior to our survey,
L. hubrichti was only known to historically occur at its type locality. Our findings extend the historical range of the species by approximately 5 river km (Fig.
3). Where found,
Lithasia hubrichti is locally abundant, particularly at the site of rediscovery (Fig.
3). Even with an extended historical range,
L. hubrichti has the smallest historical range of any non-spring-associated pleurocerid (Johnson et al.
2013; Whelan et al.
2022).
Lithasia hubrichti also has a disjunct range from other species in the genus, which could have happened via historical dispersal of
Lithasia from the Mississippi River, followed by isolation. Any future biogeographic study of
Lithasia should include
L. hubrichti and species from the Mississippi River.
In 1989, failure to find
L. hubrichti at the type locality was attributed to an upstream chemical spill (
pers. communication, Leslie Hubricht letter to USFWS, 1989). While we have no direct evidence to support claims of a chemical spill, we cannot rule it out. If a chemical spill was the reason
L. hubrichti disappeared from the type locality, at some point
L. hubrichti may have also disappeared at the lowermost site where we found the species present in 2023. If such an event occurred, it would mean that
L. hubrichti likely migrated downstream since the pollution event because pleurocerids have extremely downstream-biased migration patterns (Whelan et al.
2019; Redak et al.
2021). Yet, that scenario seems unlikely given the distributional gap between the lowest two sites where we found
L. hubrichti and given that the type locality is in-between those two sites. Instead, we think a more likely explanation is that the species was never extirpated from the lowest site, but instead not surveyed; notably the reported survey in 1989 only included the type locality (
pers. communication, Leslie Hubricht letter to USFWS, 1989). Regardless of the cause for extirpation at the type locality,
L. hubrichti remains susceptible to a single catastrophic event.
Among other pleurocerid species, the conservation status of
Lithasia hubrichti is most similar to
Leptoxis foremani and
Leptoxis compacta.
Leptoxis foremani was once thought to be extinct (Lydeard and Mayden
1995) and had a historical range that encompassed much of the mainstem Coosa River and larger tributaries like the Oostanaula River. Now, the species is federally endangered under the U.S. Endangered Species Act and known from only two sites in the Oostanaula River (Powell and Hartfield
2014). Similarly,
L. compacta is a Cahaba River drainage, Alabama, USA species that was once thought to be extinct (Whelan et al.
2012) and that was recently proposed for listing as endangered under the U.S. Endangered Species Act (U.S. Fish and Wildlife Service
2023). All three species currently persist only in a small portion of the mainstem of a major river, making them susceptible to a single, catastrophic point source pollution event. However,
L. hubrichti has a smaller current range than
Le. compacta and
Le. foremani, which occupy at least 9 and 19 km stretches of river, respectively. The known historical range of
L. hubrichti is also much smaller than
Le. compacta and
Le. foremani, which could make standard conservation techniques for
L. hubrichti more difficult. For example, locations exist within the historical range of
Le. compacta that are potential sites for reintroduction that would protect the species from a single point source pollution event, but such sites (e.g., Buck Creek in Shelby County, Alabama, USA for
Le. compacta) may require habitat improvements prior to reintroduction efforts. In contrast,
L. hubrichti lacks this assurance because sites are linearly located to one another that even if habitat at the type locality was improved to a point where reintroduction could be successful, a reintroduced population would likely be susceptible to any event that causes decline elsewhere within the known range. Given how little we know about the basic biology and ecology of
L. hubrichti, reintroductions outside its historical range should be avoided (George et al.
2009; IUCN/SSC
2013; Strayer et al.
2019). Thus, the best conservation approach for
L. hubrichti will likely be habitat protection and long-term monitoring to ensure stable population sizes. Sampling additional sites within the Big Black River drainage may also be required to fully understand its distribution.
Despite the restricted known range of
L. hubrichti, we documented considerably higher genomic diversity, as estimated by summary statistics like heterozygosity and nucleotide diversity, than what was previously documented in other imperiled pleurocerids like
Leptoxis ampla (Whelan et al.
2019),
Pleurocera foremani (Redak et al.
2021), and
Le. compacta (Wright et al.
2020). However,
L. hubrichti does not appear to harbor subpopulation genomic structure like
Le. compacta (Wright et al.
2020) and
Le. ampla (Whelan et al.
2019). Wright et al. (
2020) hypothesized that the subpopulation structure of
Le. compacta was a result of extirpated ancestral populations contributing to the overall genomic diversity of the species, and the absence of subpopulation structure may be a result of
L. hubrichti having a restricted historical range. Observed heterozygosity was lower than expected heterozygosity and F
IS was nearly 0.1 in
L. hubrichti, possibly indicating that drift and inbreeding will result in a long-term decline of genetic diversity. Nevertheless,
L. hubrichti has greater genetic diversity than other pleurocerids (see results; Whelan et al.
2019; Wright et al.
2020; Redak et al.
2021). Thus, genetic drift is unlikely to cause problems for
L. hubrichti over the foreseeable future unless exacerbated by a human-mediated bottleneck.
A formal status assessment for L. hubrichti by state and federal agencies is immediately needed as the species exhibits low population redundancy and is susceptible to catastrophic events. However, comprehensive surveys in the Big Black River drainage for L. hubrichti will not be a simple task because most locations in the drainage are remote, and ideal conditions for snail surveys (i.e., low enough water for collection by hand) make boat travel difficult. For now, research, surveys, and habitat improvements should be the focus of L. hubrichti conservation efforts.