Do native and introduced freshwater turtles compete in northern Mexico?

Determining how to prioritize resource-management interventions is hard. Conservation decision-making is often hampered by imperfect data, and rigorous monitoring to measure post-intervention outcomes is rare. These issues motivated a turtle study that my colleagues and I recently published. Although we worked in a non-Mexican study system, there are potential applications to Baja California and elsewhere in northern Mexico. Let me explain.

Our team examined the idea that the globally-invasive red-eared slider turtle, Trachemys scripta elegans, competes with the native, imperiled western pond turtle, Emys marmorata (the latter is shown in the banner photo for this post). The slider is listed as one of the world’s 100 most invasive species by the IUCN (Lowe 2000). Several experiments under captive conditions show that sliders can outcompete native turtles in the family Emydidae for a variety of resources (e.g., Cadi & Joly 2003, Polo-Cavia et al. 2011). But—and this is a big but—there was no data from wild, free-living populations. So, we decided to remove the majority of an introduced slider population (177 turtles!) from a well-studied waterway in northern California (see Spinks et al. 2003 and Lambert et al. 2013), and then monitor changes in basking habitat use and body condition of the co-occurring native western pond turtles.

A non-native red-eared slider removed from a wetland in California, USA. The red “ear” marking on this particular turtle is unusually faint.

For the full story, please check out our paper (Lambert et al. 2019). You can read and download it for free here. But the takeaway message is: yes, red-eared sliders do compete with western pond turtles at this site. That said, the full story is a bit complicated. We found a strong signal of improved body condition in the western pond turtles after sliders were removed. This suggests that the two species compete for food. The basking behavior of the western pond turtles also changed post-removal. However, this change in behavior was inconsistent with what we expected if the two species were competing for basking sites. Furthermore, the western pond turtles basked a lot less post-removal, which was somewhat puzzling. Suffice it to say that my co-authors and I would love to see replication of this study in other systems. This is where Mexico comes in!

Outside of the USA, the genus Emys is native to much of northern Baja California. There is also an endemic Trachemys (the Baja California Slider, T. nebulosus) that occurs in the southern peninsula. Plus, range-restricted freshwater emydids exist elsewhere in northern Mexico, including Trachemys gaigeae, T. taylori, and T. yaquia. All of these lineages are of some conservation concern (Turtle Taxonomy Working Group 2017), and many populations occur in small, relatively isolated water bodies in arid environments (Grismer & McGuire 1993, Grismer 2002, Valdez-Villavicencio et al. 2016). So, they could be vulnerable to invasion by red-eared sliders. Or maybe this has already happened in some cases?

Desert oasis near Mulegé, Baja California Sur, showing general habitat characteristics for some emydid turtle populations in northern Mexico.

A quick look on iNaturalist provides some clarity. The database reveals widespread, but clustered, observations of non-native sliders across northern Mexico, including Baja. Although imperfect, this information suggests that sliders now exist alongside range-restricted native turtles in the region. This raises two questions. First, are the non-native turtles having a detrimental effect on the native turtles? And if so, what are appropriate management actions to reduce this impact?

Answering these questions is a little tricky, but our recent paper provides some insight. One of our big messages is that controlling, much less eradicating, an established population of red-eared sliders is expensive and time consuming. Removing turtles is probably not a feasible approach for large, complex waterways (García-Díaz et al. 2017). Furthermore, without addressing the root cause of slider introductions (people releasing their unwanted pets), eradication or control campaigns will likely be ineffective in the long term. Nonetheless, invasion biology emphasizes the need to “catch things early.” So removing a handful of newly-introduced sliders from a small desert oasis occupied by native turtles could help prevent a minor problem from becoming a large, intractable problem.

Ultimately though, it is still unclear how harmful sliders actually are to native turtles in Mexico. Our California study is the first to look at whether sliders compete with native turtles in the wild. Are our results transferable to other sites, and to other native turtle species? Additional field experiments with pre- and post-removal monitoring are desperately needed! Fortunately, readers of this blog are perhaps best positioned to identify logistically-suitable places for such tests in Mexico. Such research is critical for figuring out the best way to prioritize our limited resources. Defensible turtle-management interventions depend on it.

My hope here is to help raise awareness of the need for rigorous evidence to support proposed management strategies. And perhaps spark ideas for new science that could improve Mexican turtle conservation practices. Please consider sharing your thoughts in the comments! We’d love to hear from you.

 

Literature Cited

Cadi A, Joly P. 2003. Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Canadian Journal of Zoology 81:1392–1398

García-Díaz, P., D. S. L. Ramsey, A. P. Woolnough, M. Franch, G. A. Llorente, A. Montori, X. Buenetxea, A. R. Larrinaga, M. Lasceve, A. Álvarez, J. M. Traverso, A. Valdeón, A. Crespo, V. Rada, E. Ayllón, V. Sancho, J. I. Lacomba, J. V. Bataller, and M. Lizana. 2017. Challenges in confirming eradication success of invasive red-eared sliders. Biological Invasions 19:2739–2750.

Grismer, L. L. 2002. Amphibians and Reptiles of Baja California, Including its Pacific Islands and the Islands in the Sea of Cortés. University of California Press, Berkeley.

Grismer, L. L., and J. A. McGuire. 1993. The oases of central Baja California, México. Part I. A preliminary account of the relict mesophilic herpetofauna and the status of the oases. Bulletin of the Southern California Academy of Sciences 92:2–24.

Lambert, M. R., S. N. Nielsen, A. N. Wright, R. C. Thomson, and H. B. Shaffer. 2013. Habitat features determine the basking distribution of introduced red-eared sliders and native western pond turtles. Chelonian Conservation and Biology 12:192–199.

Lambert, M. R., J. M. McKenzie, R. M. Screen, A. G. Clause, B. B. Johnson, G. G. Mount, H. B. Shaffer, and G. B. Pauly. 2019. Experimental removal of introduced slider turtles offers new insight into competition with a native, threatened turtle. PeerJ 7:e7444.

Lowe S, Browne M, Boudjelas S, De Poorter M. 2000. 100 of the World’s worst invasive alien species. A selection from the global invasive species database. The Invasive Species Specialist Group (ISSG) of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), 12.

Polo-Cavia N, Lopez P, Martin J. 2011. Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions 13:1387–1396

Spinks, P. Q., G. B. Pauly, J. J. Crayon, and H. B. Shaffer. 2003. Survival of the western pond turtle (Emys marmorata) in an urban California environment. Biological Conservation 113:257–267.

Turtle Taxonomy Working Group [A. G. J. Rhodin, J. B. Iverson, R. Bour, U. Fritz, A. Georges, H. B. Shaffer, and P. P. van Dijk]. 2017. Turtles of the World: Annotated Checklist and Atlas of Taxonomy, Synonymy, Distribution, and Conservation Status (8th Ed.) inA. G. J. Rhodin, J. B. Iverson, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, P. C. H. Prtichard, and R. A. Mittermeier, editors. Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs 7:1–292.

Valdez-Villavicencio, J. H., A. Peralta-García, and J. Á. Guillen-González. 2016. Nueva población de la tortuga de poza del suroeste Emys pallida en el Desierto Central de Baja California, México. Revista Mexicana de Biodiversidad 87:264–266.

Not-so-ugly ducklings

In North America and temperate regions of Mexico, lizards in the genus Sceloporus sometimes get a bum rap. Known as fence lizards or spiny lizards in the vernacular, these squamates are typically dull-colored, sporting a mixture of brown, tan, and gray hues. As a consequence, they are often afforded little attention in the field. Some exceptions certainly exist. Sceloporus minor, with its neon blue-and-orange patterning, springs readily to mind. As do the colorful (and unusually hefty) S. cyanogenys, S. orcutti, and S. magister. But the stereotype holds…and almost none are bright green.

Sceloporus orcutti (left) and S. magister (right).

This changes in the tropical regions of Mexico, particularly in mesic montane woodlands. Within these forests, vibrant green Sceloporus, sometimes with turquoise and yellow highlights, become the standard. As hinted at earlier on this blog, many of these lineages belong to the formosus group, where species boundaries are frustratingly muddled. Teasing apart what’s going on could be a great graduate project! Interestingly, members of this group also show strong affinities for climbing in trees—so their color might be related to crypsis.

To demonstrate what I’m talking about, below I share a small sampling of striking green Sceloporus.

Sceloporus formosus, El Sumidero, Veracruz

Sceloporus megalepidurus, El Sumidero, Veracruz

Sceloporus grammicus, Altotonga, Veracruz

Throughout the entire genus, sexual dichromatism is the rule. Males are typically much more strikingly colored than females. Particularly on the belly, where patches of contrasting blue, black, and even yellow or red color serve to advertise the males’ vigor. So full disclosure: all individuals illustrated in this post are males.

Do other readers have Mexican Sceloporus experience? If so, we’d love to see your images and learn more about the diversity in this fantastic clade!

Now you see me, now you don’t

There are a whole host of reasons why anguid lizards are cool. But among the most fascinating is their tendency to change color as they age. This shift can be subtle, as in certain Elgaria. But it reaches an extreme in some Abronia. For taxa that are bright green as adults, the neonates/juveniles are so dissimilar that to the uninitiated, it can be hard to believe they are conspecific!

Why does this age-related color change (ontogenetic variation) exist? The short answer is that nobody really knows. In extraordinary cases like the A. graminea illustrated above, we can hypothesize that it represents an adaptation for microhabitat specialization. Perhaps the babies select lichen-covered twigs and branches, while the adults occupy a niche dominated by leafy growth. Based on radio telemetry data (forthcoming soon!) we do know that A. graminea adults spend virtually all of their time, at least during the breeding season, in the forest canopy. But there are no studies on where neonate/juvenile Abronia like to hang out—in large part because they are so hard to detect in the first place. Juveniles are unknown to science for over half of all Abronia species.

At first glance, especially when placed on a contrasting background, it might seem that the green color of some adult Abronia is so striking, so vibrant as to interfere with their camouflage. Nothing could be further from the truth. Set against the verdant foliage of the cloud forests they inhabit, these lizards disappear like ghosts. Can you find the one A. graminea in each of the photos below? If not, you’re in good company. I too would have been wholly unaware of them were it not for the signal coming from their “fanny pack” radio transmitters!

If readers have photos of other Mexican anguids that showcase ontogenetic variation and/or camouflage, please consider posting! We’d enjoy hearing from you.

How Many Green Dragoncitos?

In my last post I offered a brief introduction to Abronia biogeography, and highlighted some of the problems facing those who study this group. Here, I’d like present the interesting case of A. matudai and A. smithi. My hope is to draw some attention to an overlooked taxonomic quandry, and perhaps stimulate readers to consider Abronia for their future work in Mexico!

Both A. matudai and A. smithi are chronically understudied. They are endemic to the Sierra Madre de Chiapas mountains, and each is known from fewer than 10 localities rangewide. Both exemplify the archetypal dragon-like image that people sometimes associate with Abronia—bright green in color and often with enlarged supra-auricular scales or “horns” behind their ears. Although based strictly on morphological evidence (published DNA sequence data is available only for A. matudai), both are considered members of the Auriculabronia clade. This is one of six currently recognized groups within the genus.

Perhaps the most obvious external difference separating these two species is that A. smithi has dramatic spine-like supra-auricular scales, while in A. matudai the supra-auriculars are only somewhat protuberant and not pointed like spines. A handful of other external features separate them, but it could be argued that these two taxa are not strongly differentiated morphologically. In their classic monograph published a quarter-century ago, Drs. Jonathan Campbell and Darrel Frost first elevated A. smithi from within A. ochoterenai (a story for another day!). Those authors examined a total of ten A. smithi specimens and four A. matudai specimens in making their taxonomic determination. Since then, novel material attributed to both species has trickled into a few museums, but no detailed data on these specimens has ever been published. It is thus an open question whether analysis of this new material would support, or soften, the presumed morphological divergence between these two taxa. Based on my collaborative recent work with other members of the genus, the latter option might be more likely.

A close look at regional geography raises further questions. Currently, A. matudai is known to occupy an elevational range of ca. 1540–2700 m, while A. smithi is reported from 1580–2800 m elevation. Both species inhabit “cloud forest,” a rather nebulous term that can encompass a wide diversity of forest types. While perhaps an oversimplification given that elevation is not a perfect proxy for Abronia habitat, one might reasonably assume the existence of a low-elevation barrier to dispersal between these two taxa. The deep entrenchments of the Río Coatan and Río Huixtla, at first glance, appear to fit the bill. However, in reality a narrow montane corridor in excess of 1900 m spans the headwaters of these rivers, connecting the escarpments occupied by A. matudai to the east and A. smithi to the west. As such, there is no obvious geographic barrier to gene flow.

So, is A. smithi valid? Or could it perhaps represent a clinal extreme of A. matudai? And could there be one or more cryptic, undescribed lineages clouding the issue?

Just some of the many Abronia questions waiting to be answered…please comment below with any feedback!

Our Evolving Understanding of Abronia Biogeography: Problems with the Allopatry Narrative

As many readers are aware, I spend a lot of time (too much time?) thinking about arboreal alligator lizards in the genus Abronia. These squamates are fascinating for a litany of reasons. They are physically striking animals, they possess an air of mystery due to their secretive tree-dwelling behavior, and they live in remote, inaccessible “sky islands” of habitat. We have much to learn, and this makes them an exciting group to study.

A sampler of Mexican species of Abronia                                                                           From top: A. bogerti, A. taeniata, and A. graminea.

The 29 described species of Abronia are also emerging conservation flagships for imperiled Mesoamerican cloud forests. Most major mountain ranges between central Mexico and western Honduras support their own unique, range-restricted Abronia. Some species, in fact, are known to science from just a single cloud forest peak. Allopatric speciation is thus considered the dominant pattern in their evolutionary radiation—in any given forest, on any given mountain, you’ll find just one Abronia species.

Or at least, that was the conventional wisdom until recently. Things are changing. The acquisition of new field data has taught us that about one-third of Abronia actually occur in sympatry with a congener. The maps below provide a big-picture overview.

But let’s explore what’s happening in these maps more closely. In eastern Mexico’s Sierra Madre Oriental, there is a 100-km zone of sympatry between A. graminea and A. taeniata. Reduced morphological differentiation in this zone, together with ongoing genetic work, suggests the possibility of gene flow; conversely, one or both taxa might harbor as-yet unidentified cryptic species-level lineages—the exact story remains unclear. Farther to the south in the Mexican state of Oaxaca, there are remarkable reports of A. mixteca and A. oaxacae (or at least, animals morphologically consistent with those two species) being found on the same tree. Elsewhere in Mexico, on opposite sides of the Isthmus of Tehuantepec, members of the Scopaeabronia clade are paired with members of the Abaculabronia clade. Available records indicate that the two largest volcanoes in Los Tuxtlas support both A. chiszari and A. reidi, and that Cerro Baúl in the Chimalapas highlands supports both A. bogerti and A. ornelasi in overlapping elevation bands. Turning to Guatemala, recent sampling has shown that the distantly-related A. frosti and A. lythrochila occur within 5 km of each other on the same flank of the Sierra de Los Cuchumatanes. Farther to the east, a 50-km arc of Guatemala’s Sierra de Xucaneb mountains is occupied by populations of both A. fimbriata and A. gaiophantasma. Suspected, but as-yet unconfirmed sympatry may also exist between A. fuscolabialis/A. mitchelli and A. cuetzpali/A. oaxacae in different regions of Oaxaca, Mexico.

Now hold on a minute, you might be saying. Sympatry is one thing. But what about syntopy, where multiple species occupy the exact same spot (in this case, the exact same trees)?

The answer is that out of the six confirmed sympatric species pairs, syntopy has actually only been documented in two: A. mixteca/A. oaxacae and A. fimbriata/A. gaiophantasma. So, many sympatric Abronia might still plausibly be considered niche-segregated, due to the heterogeneous forest mosaic on Mesoamerican mountains. Countering that argument, however, is growing evidence that individual Abronia species can inhabit a wider range of elevations and forest microhabitats than previously believed. For instance, in the past two years A. taeniata has been found at the bizarrely low elevations of 125 and 300 m in Hidalgo, Mexico. These and other observations emphasize that slope, aspect, soil composition, and prevailing moisture-bearing winds all combine to create a wondrously complex patchwork of montane forest niches. Elevation alone can’t explain things perfectly. Coupled with field sampling difficulties, this situation continues to challenge efforts to draw accurate, fine-scale conclusions about where Abronia exist on the landscape.

Suffice it to say, the biogeographic story of Abronia evolutionary diversification and habitat occupancy has become a lot more problematic lately. Nonetheless, we can apply these lessons to help resolve, or at least draw attention to, some troublesome taxonomic situations in the Abronia Tree of Life. Stay tuned for an upcoming post exploring one such case.

What does “versant” mean in the context of biogeography?

Words matter. More specifically, the conventional meaning ascribed to words matters. I have been struggling with this in the context of some Mexico research this week. As a neophyte to biogeography, I wanted to solicit feedback from sage readers on this blog more experienced than myself. So, basically…all of you!

Allow me to set the stage.

Let’s take the Sierra Madre de Chiapas. For those who are unfamiliar, this is a northwest–southeast trending mountain range in Mexico and Guatemala which, in the Mexican state of Chiapas, tightly parallels the Pacific Ocean. The ragged peaks tower dramatically above the narrow coastal plain. Some might argue that it’s the coolest mountain range in Mesoamerica…but that’s a subject for another post! For most of its length in Chiapas, the western foothills of the Sierra Madre de Chiapas are less than 30 km from the Pacific Coast. But the eastern slopes, which eventually drain into the Gulf of Mexico, lie closer to 300 km from the Gulf. To put it another way, in Chiapas, the Continental Divide runs along the spine of the Sierra Madre de Chiapas. Rainfall to the west of the crest drains into the Pacific, via a short and direct route. Rainfall to the east of the crest drains into the Gulf, via a long and circuitous route.

Now let’s say that a species (to keep things interesting, let’s make it an emerald-green snake) occurs on both the eastern and western slopes of the Sierra Madre de Chiapas. To clarify, I am not talking about occurrence records that lie just a few dozen meters northeast (toward the Gulf) from the crest of the mountains. I am talking about records that lie multiple km away from the line where precipitation drains into the Pacific instead of the Gulf.

So, here’s my question: can the geographic range of this species accurately be described as a “Pacific versant distribution”? Put another way…does the word “versant” refer to the set of points on a map where rainfall drains into a particular ocean? Or does it refer to the set of points on a map that are all closer, in Euclidean distance, to a particular ocean?

The motivation behind my question is as follows. It appears that authors have long been misusing the phrase “Pacific versant“ when describing the distribution of the species in question. However, I am looking for independent confirmation of this suspicion before I (gently) call attention to those presumed mistakes.

Please share your thoughts in the comments! And because this is a dry topic, here is a photo of the species that may have motivated this post.