Evolution and conservation in Mexican dry forests

The characteristic peeling bark of Bursera simaruba. Copyright Kurt Stueber, licensed under the GFDL

Bursera simaruba has always been one of my favourite tree species. It’s a dry-season deciduous tree with compound leaves and a coppery peeling outer bark and a green (presumably photosynthetic) inner bark.  It’s a conspicuous element of tropical dry forests in Trinidad and Tobago, Puerto Rico and parts of southern Florida (where they call it the ‘gumbo limbo’ tree).  In all these places it’s the only representative of its genus.  In my experience, Bursera was Bursera simaruba, so I was surprised when I came across a Bursera that was grown from seed collected in Costa Rica that was obviously not B. simaruba.  Nonetheless, I still thought of Bursera as a relatively small genus.  Then I came across some information on the genus in Mexico which turned my picture of Bursera completely on its head.  There are 84 species of Bursera in Mexico – 80 of which are endemic – out of a total of approximately 100 species in the genus.  So why are 80% of the species of Bursera – a genus which ranges from Florida to Argentina – restricted to Mexico?

Species diversity patterns reflect several underlying processes – those that generate diversity, and those that maintain that diversity.  When species are grouped into a genus, the assumption is that they are more closely related to one-another than are they to any species in a different genus.  To get from that one ancestral species to its modern descendants, something must occur that allows the single ancestral lineage to split into several daughter lineages (a process known as speciation).  This figure from the Wikipedia article on speciation summarises the different modes of speciation.

In order to generate the type of pattern seen in Bursera, you need one of two evolutionary processes to be active.  Either Bursera originally diversified in Mexico, and a few species have spread beyond that ancestral range (giving rise to their own daughter species along the way) or something happened in Mexico that led to the diversification in a limited portion of the range of a widespread genus.  In the former case, Mexican diversity should be old, and the splits between the Mexican species should lie deep in the ancestry of the genus.  In the latter case, Mexican diversity is newer, and the splits between the Mexican species are likely to have been derived from more widespread species.

In a paper published in PLoS ONE in October, Judith Becerra and Lawrence Venable of the University of Arizona looked at the case of Bursera in Mexico.¹ Bursera is an old genus – molecular phylogenies based on ribosomal DNA suggest that modern species share a common ancestor about 66-74 million years ago, and fossil evidence suggests that the genus was once ranged over a much wider portion of North America.² It turns out that most of the Mexican species are more recent.  The number of lineages increased substantially within the last 30 million years³ and peaked between 10 and 17 million years ago (which coincides with the formation of the Western Sierra Madre and the Neovolcanic belt).¹ Becerra suggested that the diversification of Bursera is likely to have coincided with the expansion of dry forests in central and southern Mexico.³ These dry forests were made possible by the uplift of the mountains which provided appropriate climatic conditions for the establishment of tropical dry forests by sheltering them from northern cold fronts.¹

In previous work, Becerra has built a detailed phylogeny of the Mexican species of Bursera.  Using this phylogeny, she was able to show that the diversification of these species coincided with the formation of the Western Sierra Madre and the Neovolcanic belt.  In the PLoS ONE article she and Venable used this phylogeny and the distribution of existing Bursera species to predict where the various species are likely to have originated.  Despite the fact that it ranks third in Bursera species richness today, they found that the Southwest was actually the source of the largest number of species.  The Balsas River basin, on the other hand, has the most species (and the largest number of endemic species), but was the site fo relatively few diversifications.  Continued mountain-building led to an expansion of dry forest, into which new species wer able to spread.  Other new species were able to invade the Mexican highlands, the Sonoran Desert, upland oak forests or subhumid tropical forests.

Becerra and Venable termed the diversity-generators “source” areas and the non-dry forest habitats as “diversity sinks”.  Personally, this bothered me, as it felt like they were borrowing terminology from population ecology (where it applies to individuals within populations) and applying it to species in a way that is likely to bring unwanted baggage.  Sink populations recruit fewer individuals than are required to replace losses to the population, and as such will go extinct if they don’t continue to receive immigrants from the source population.  There’s nothing to indicate that Becerra and Venable are using ‘sinks’ to mean anything beyond the fact that these areas are occupied by species that evolved elsewhere.  Using this borrowed terminology is likely to mislead readers who are more familiar with the concept of source-sink dynamics in population ecology.

Since certain areas have been superior generators of diversity, Becerra and Venable suggest that prioritising them for conservation should yield superior long-term outcomes.  Protecting areas that can generate diversity should be more important than simply protecting areas that harbour greater diversity.  They write:

The differences between diversity and diversification mean that this may be transitory in the long run, analogous to protecting species in zoos. While it might sound unusual to try to conserve diversity based on events happened in the past, there may be cases in which the aerographic patterns of diversification have occurred repeatedly for a long time, giving us some kind of assurance that it will continue happening in the same way for at least the near future. In the case of Bursera, diversification seems to have been higher in one area for a long time, starting 15 million years ago or perhaps even longer. If not greatly perturbed, there is no reason not to believe that these same patterns of diversification will continue. This approach could be especially useful if there are no other stronger criteria to decide where conservation efforts should be directed. If we had to choose between conserving one of two areas and everything is equal except their history of being sinks or sources of diversification, there would be no harm and perhaps much gain in choosing the source. The long-term maintenance of biodiversity require us preserve its sources, to the extent that these can be accurately determined [8].

[Emphasis added]

I’m not sure if I agree, or disagree.  On one hand, there’s a lot of evidence that suggests that species assemblages are more transient than they were assumed to be in the past.  The simple fact that an area supports a large assemblage of species may reflect chance as much as some special property of the site.  So from that perspective, the areas that have generated diversity should be more important than the areas that harbour diversity.  On the other hand, why should we assume that an area that generated a lot of diversity in the past will continue to do so in the future?  The rate at which new species are being generated appears to have declined sharply in past 10 million years.³ If, as has been suggested, the generation of diversity was related to mountain-forming, is it reasonable to expect the process to continue?  It’s difficult to say what it is that generates a species flock in one area and not in another.

The other big question I found myself with was what is the purpose of conservation?  At what point will we be able to stop protecting species and environments?  When will the threats recede, or will they recede at all?  What will the world look like when the current human-driven extinction event has run its course?

This post is my contribution to PLoS ONE @ Two, a celebration of the second birthday of PLoS ONE.

1. Judith X. Becerra, D. Lawrence Venable (2008). Sources and Sinks of Diversification and Conservation Priorities for the Mexican Tropical Dry Forest PLoS ONE, 3 (10) DOI: 10.1371/journal.pone.0003436
2. Judith X. Becerra (2003). Synchronous coadaptation in an ancient case of herbivory.  Proceedings of the National Academy of Sciences USA 100 (22): 12804-12807 DOI: 10.1073/pnas.2133013100
3. Judith X. Becerra (2005). Timing the origin and expansion of the Mexican tropical dry forests.  Proceedings of the National Academy of Sciences USA 102 (31): 10919-10023 DOI: 10.1073/pnas.0409127102

Disturbance and recovery in tropical dry forests

When people think about the destruction and degradation of tropical forests, they tend to focus on rainforests. Tropical dry forests tend to get overlooked. They aren’t as striking – no cathedral-like understorey, no mind-boggling biodiversity. But more importantly, they often just aren’t there. Over much of their potential range they have simply been erased from the landscape. They may have covered as much as 42% of the land area in the tropics¹, but have been reduced to less than 27% of their former range in Mexico², and as little as 2% in Central America³ and New Caledonia⁴.

Despite the fact this, tropical dry forests are often seen as being quite well-adapted to human disturbance. Being less species-rich than wetter forests, they tend to support fewer rare species, and may be less extinction-prone. In addition, dry forests are dominated by trees that sprout after being cut. This means that if you cut down a patch of dry forest, most of the stumps will re-sprout. This type of recovery is much quicker than you would get if the trees had to germinate from seeds – not only does it take much longer for seedlings to grow large (stump sprouts can draw on resources stored in the roots of the tree), but there’s likely to be a time lag as seeds disperse into the area from surviving trees (tropical forests tend to lack long-lived seedbanks).

Much of our understanding of succession in tropical dry forests comes from Jack Ewel’s dissertation work. Ewel looked at the effect of cutting and herbicide application on succession in a series of plots across the Neotropics. One of his important findings was the dry forests were quicker to recover their stature that wetter forests. Since most of the recovery comes from stump sprouts, the recovering forest is also close to the original forest in terms of species composition.

While lightly used dry forest sites recover rapidly, recovery is slower in more intensively used sites. Seedling survival rates are very low in dry forests – while seedlings establish in the wet season, most (often all) of them die in the subsequence dry season. So while intensively used sites in Guánica Forest recovered well in terms of structure, biomass and leaf fall in 50 years after abandonment, the recovery of species composition was very slow⁶.

Resilience is the rate of recovery of disturbed sites to their pre-disturbed state. Ewel’s work helped to establish the idea that dry forests are more resilient than wetter forests. But there is no single rate – or pathway – of recovery. Measures of “recovery” depend on the parameter measured – canopy height, biomass, species richness, nutrient cycling… It also depends on the baseline against which recovery is measured: if the same site is measured before and after disturbance, you need to know if the site represented “mature” forest before disturbance. If another site is used, you need to wonder if it is really representative of initial conditions in your experimental plot.

In a forthcoming paper⁷ in the journal Biotropica, Edwin Lebrija-Trejos and coauthors looked at what it really means to say that tropical dry forests are more resilient than wetter forests. They looked at a sequence of 15 sites in Oaxaca, Mexico, which had been cultivated and then abandoned for 0-40 years, and compared them with nearby mature forest. All of the sites had been cultivated for a short period (1-2 years) and then abandoned without being converted to pasture⁸. They considered a variety of different ways to measure resilience – they looked at forest height, plant density, basal area (the area occupied by tree stems), crown cover, species richness, species density (number of species per 100 m²), Shannon evenness and Shannon diversity. Not surprisingly, they found that certain features (canopy height, plant density, crown cover) recovered rapidly (in less than 20 years) while others (including basal area and species richness) had not recovered after 40 years.

When compared their sites with other comparable studies, they found that their sites were among the quickest to recover canopy cover and height. On the other hand, they found that their sites were among the slowest to recover species diversity and average in terms of the recovery of species richness. Overall, in terms of the structural measures that Ewel focussed on, it’s reasonable to conclude that dry forests are more resilient that wetter forests. On the other hand, with regards to things like basal area and species richness, the assertion of resilience for dry forests isn’t well supported.

1. Brown, S., and A. E. Lugo. 1982. The storage and production of organic matter in tropical forests and their role in the global carbon cycle. Biotropica 14:161-187.
2. Trejo, I., and R. Dirzo. 2002. Floristic diversity of Mexican seasonally dry tropical forests. Biodiversity and Conservation 11:2063–2084
3. Janzen, D. H. 1988. Tropical dry forests: The most endangered major ecosystem. In E. O. Wilson (Ed.). Biodiversity, pp. 130–137. National Academy Press, Washington, DC
4. Gillespie, T. W., and T. Jaffré. 2003. Tropical dry forests in New Caledonia. Biodiversity and Conservation 12:1687–1697.
5. Ewel, J. J. 1971. Experiments in arresting succession with cutting and herbicide in five tropical environments. Ph.D. University of North Carolina, Chapel Hill.
6. Molina Colón, S., and A. E. Lugo. 2006. Recovery of a subtropical dry forest after abandonment of different land uses. Biotropica 38:354–364.
   
7. Lebrija-Trejos, E., Bongers, F., Pérez-García, E.A., Meave, J.A. (2008). Successional Change and Resilience of a Very Dry Tropical Deciduous Forest Following Shifting Agriculture. Biotropica DOI: 10.1111/j.1744-7429.2008.00398.x
8. Conversion to pasture tends to slow recovery significantly; not only does the prolonged period eliminate almost all root stocks, it also establishes a grassy layer that makes it more difficult for tree seedlings to establish.

A remarkable new palm from Madagascar

As a result of its long isolation, Madagascar has unique biota. Although it is best known for its lemurs, Madagascar’s palm flora is both diverse and distinctive. In 1995 Dransfield and Beentje recognised 170 species of palms from Madagascar, 164 of which were found only in Madagascar. Since then another 7 species have been described, with another 20 apparently awaiting description. Most of these new species have been found in the eastern wet areas. The western part of the island is drier, and has a much less diverse palm flora. However, an entirely new genus has been discovered in the western dry region – one that is so large and distinctive that the BBC reports it can be seen in satellite images. A description of this new species, Tahina spectabilis was published in the January issue of the Botanical Journal of the Linnean Society.

Tahina, which means “blessed” or “to be protected” in Malagasy (and is also the name of the daughter of the Metz family, Anne-Tahina), is a remarkable tree. It is one of the largest palms in Madagascar, growing 10 m tall (20 m according to the BBC article) with stem diameter of 50 cm. It is also hapaxanthic – it reproduces just once in its lifetime and then dies. As a result of this, it puts all of its resources into flowering, producing a 4-m tall inflorescence. (You can see an image of it here.)

In August 2005 the Metz family first observed the species on a family picnic, but since it was not flowering, they assumed that it was a Borassus. However, when they returned in 2006 they saw the tree in flower. Their pictures were posted on the PalmTalk bulletin board by Bruno Leroy on December 5, 2006, where its similarity to the Asian genus Corypha was noted. One of the regulars on the board contacted John Dransfield of Kew Gardens, who determined that the species was not a Borassus, and thought that it was unlikely to be a Corypha, since the area appeared to be too remote for one to have been planted there. Images of the crown were also inconsistent with Corypha. Corypha (the Talipot Palm) has a similarly massive terminal inflorescences (picture, on right) and has been planted around the world. I have seen them in flower in Trinidad and Puerto Rico, and one of them in flower is a truly remarkable sight.

In January 2007 Mijoro Rakotoarinivo, Bruno Leroy and the Metz family visited the site and made the first botanical collections of the species. The species was determined to be an unknown member of the tribe Chuniophoeniceae which comprised of three genera: Nannorrhops, which is found from Arabia to Afghanistan, and Pakistan; Kerriodoxa which is found in southern Thailand; and Chuniophoenix which is found in Vietnam and southern China. Unlike Tahina, these genera are slender or moderate sized palms. In addition to being physically distinctive, Tahina is also geographically disjunct from its closest relatives.

Apart from everything else about this tree, I especially like the internet aspect. Certain taxa, like palms and fish, support dedicated communities of enthusiasts. Their interest can not only lead to new discoveries, it can also be harnessed into research and conservation efforts. And, remarkably, they generate groups of non-scientists who actively read taxonomic monographs. And to me, that’s just awfully cool.

Dransfield, J., Rakotoarinivo, M., Baker, W.J., Bayton, R.P., Fisher, J.B., Horn, J.W., Leroy, B., Metz, X. (2008). A new Coryphoid palm genus from Madagascar . Botanical Journal of the Linnean Society, 156(1), 79-91. DOI: 10.1111/j.1095-8339.2007.00742.x

Dransfield J, Beentje HJ. 1995. The Palms of Madagascar. Royal Botanic Gardens Kew and International Palm Society, HMSO Norwich.

Guayanilla Windfarm EIS: Puerto Rican nightjar I

The proposed Windmar RE windfarm near Guayanilla occupies habitat of Caprimulgus noctitherus, the Puerto Rican nightjar or Guabairo. As a result of this, the Environmental Impact Statement addresses the potential impact of the project on this species. A consultant’s report* was prepared on behalf of Windmar RE by Paul Kerlinger of Kerlinger & Curry LLC. documenting surveys carried out in 2003, and a follow-up memo* from Kerlinger details additional surveys carried out in 2004. These results are also discussed (in more rosy terms) in the Habitat Conservation Plan**

Kerlinger and associates surveyed the site in 2003 and again in 2004, and estimated that there were 33 nightjar territories on the site in 2003 and 46 territories in 2004. Kerlinger attributes this increase to one of three causes

1. That the observers had become better at finding birds;
2. That there was an overall increase in the nightjar population; or
3. That “the access roads that have been cut through the forest at the WindMar site provided better foraging habitat such that more territories could occupy the site”

Kerlinger favours the third explanation – that the construction of roads opened up the canopy, making foraging easier for the birds. He also says that “the trails at the WindMar site may now provide better foraging habitat that actually attracts nightjars from other areas or permits them to live on smaller territories by making foraging better.” He supports the assertion with a few anecdotes, including:

On one night at the Punta Ventana property, where more access roads were established, the data collection team reported an adult with two recent fledgling nightjars foraging along one of the access roads, and another older fledgling foraging along another.

In all of these, Kerlinger fails to consider a variation of (1) – that construction and widening of roads makes it easier for researchers to move through the forest and may change their perceptions of the direction and distance of bird calls. Dry forests are difficult to move through in the night. While narrow trails had been cut for the 2003 survey, wider trails make for easier access, and allow the observers to travel more quietly. It is rather curious that Kerlinger neglected to address this possibility. In addition, his anecdotes about observing adults with fledglings is really pretty meaningless – basically he says that, once the roads were cut, he was able to see fledglings along the roads. Is it really worth mentioning that the presence of roads makes it easier to see animals along roads?

In discounting the idea of population increase, Kerlinger suggests that “[i]t is important to note that the density of nightjars on a per hectare basis was higher on the Wind Mar project site than has been reported in most parts of Puerto Rico. Given the high density, one would expect birds to disperse to other locations rather than become even denser at the Wind Mar site.” In the Habitat Conservation Plan Guarnaccia expands on this by noting “Besides, singing territory size did not decrease as one would expect in more densely packed habitat (Weeden 1965). Instead, it appeared to increase slightly.” Guarnaccia uses this to argue in favour of the idea that increased road density has improved the habitat for nightjars.

I find this rationale puzzling. As Guarnaccia indicates, as density increases, territory size usually shrinks. Territory size tends to be driven by two things – access to food, and competition with conspecifics. Competition with other animals consumes resources, so it’s unprofitable to fight for more territory than you absolutely need. But if you don’t have enough territory to raise your offspring, then there is a strong impetus to compete for additional territory. If you can’t secure enough territory at a site, then you are likely to look elsewhere.

If the construction of the roads increased the resource base and led to an increase in population size, then you would expect territory size to shrink. An increase in territory size (assuming it is real) is more likely to be driven by a decline in habitat quality. It is the opposite of what you would expect given an improvement in habitat quality. Therein lies the problem – it is unreasonable to use the same explanation for conflicting observations. While increased population density is consistent with the explanation favoured by Guarnaccia and Kerlinger, increase territory size is inconsistent with that explanation. While there isn’t enough data to distinguish between an observer effect or a real population increase, I think it’s reasonable to reject Kerlinger and Guarnaccia’s explanation, based on the data provided.

It’s possible to attribute the observations to either an observer effect or a real population increase. An increase in the number of territories is consistent with a road effect: better access made for better surveys. On the other hand, an increase in population size (or degradation of habitat elsewhere) would result in additional territories being occupied. Increased territory sized (if the increase is real and not just a statistical artefact) would be consistent with habitat degradation (perhaps as a consequence of road construction).

What’s more important in all this is that they have only presented two years of data. Two data points will always appear to show a trend, whether one exists or not. But the reality is that it takes a minimum of three data points to be able to say anything about your estimate. Kerlinger emphasises that their sampling intensity was greater than that of Vilella and Zwank. While an increase in nightjar population over the last two decades is reasonable (based on sightings in the last few years which suggest range extensions), it is also possible to attribute these to increased awareness of the species leading to an increased observer effect.

It turns out that I am not the only one unimpressed with Curry and Kerlinger’s work (scroll down to the story after the one about this project).

————————

*Kerlinger, Paul. 2003. A Preconstruction Study of Abundance and Distribution of the Federally Endangered Puerto Rican Nightjar at the WindMar Re Project, Guayanilla, Puerto Rico;
Kerlinger, Paul. 2004. 2004 Territorial Boundaries of Puerto Rican Nightjars at the WindMar Project Site in Guayanilla, Puerto Rico.

**Guarnaccia, John. 2005. Final Draft: Habitat Conservation Plan. WindMar RE Project Guayanilla, Puerto Rico

Other posts on the subject:

• Guayanilla Windfarm – general thoughts on the topic.
• Species-area curves – when they get the get the most basic biology so badly wrong, you tend to lose confidence in what they have to say rather rapidly.

Guayanilla Windfarm EIS: species-area relationships

The proposal by WindMar RE to build a windfarm at Punta Verraco, Cerro Toro and Punta Ventanas in southwestern Puerto Rico has generated controversy (see my first post on the issue) on a number of issues. One of the things that bothers me most is the sloppy Environmental Impact Statement. I have not read the whole thing, but the biological aspects are disturbingly bad.

One of the most fundamental issues in ecology is the species-area curve. Species richness increases with area (but not linearly). Larger areas have more species. On a certain level this in intuitively obvious – the smallest possible area has one individual, so it can only have one species. If you expand your sample to include two individuals, you may find that the second individual belongs to the same species, or you may find another species. If every new individual encountered was a member of a new species, you would have a line with a slope = 1. In reality though, you are almost certain to encounter more than one individual of at least some of your species, so your curve will flatten a little bit. (What I am describing is a species-individual curve rather than a species-area curve, but similat rules apply for area.) One of the fundamental points that comes from this is that larger areas will contain more species. This is one of the most basic relationships in ecology. Anyone who has any background in ecology knows this. Unfortunately, this seems to have slipped the mind of the authors of the Habitat Conservation Plan (p. 27):

So far, botanists have recorded nearly 170 species of vascular plants at the
WindMar site (see Appendix II), a diversity far below the over 700 species recorded in the Guánica State Forest. … This confirms hat the dry forest plant community on the WindMar site is poor and has been severely impacted. A management plan to help these forests recuperate is clearly in order.

Guánica Forest occupies about 4000 ha. The site in question occupies 290 ha. No one would expect the site to have anywhere near the number of species than Guánica Forest has. However, if you examine the species list (p. 13) you will see that it lists 168 species from Punta Verraco, which accounts for only 43% of the site (125 ha; Habitat Conservation Plan, p. 24). In addition, the authors of the report cite no sources for their figure of “over 700 species” recorded for Guánica Forest – the most recent source I am aware of lists a little over 650 species. Regardless, what this accounts for 24-26% of the species recorded for Guánica Forest in about 3% of the area. Add to that the fact that the species list for Guánica Forest includes habitats not represented in the survey, and you end up coming to the conclusion that species diversity of this site is very high.

When the authors of the report get the most basic biology so badly wrong, you tend to lose confidence in what they have to say rather rapidly.

Other posts of mine on the subject:

• Guayanilla Windfarm
• Puerto Rican nightjar, part I.

Guayanilla Windfarm

As power generation schemes go, I have mixed feelings about wind farms. Obviously they have huge advantages over fossil fuel-powered plants. They also don’t involve damming rivers. But they are not without impacts – they tend to be death traps for birds, and they are visually unappealing.

There will always be trade-offs, and given how serious an issue climate change is I am probably willing to tolerate compromises that I would otherwise consider totally unacceptable (nuclear power being one such). But the spirit of compromise is to find the best way to balance various competing ideas. It’s quite different when you are faced with one of the worst possible scenarios. Plans to construct a wind farm in Guayanilla, Puerto Rico seems to be one of the latter. Not only is it located in prime habitat for a federally listed endangered species (Caprimulgus noctitherus, the Puerto Rican nightjar), it also intrudes into high quality dry forest immediately adjacent to Guánica Forest, the most important remaining tract of dry forest in Puerto Rico.

Having looked at the Environmental Impact Statement I am also shocked at the quality of it. Not only do the authors appear to know nothing about dry forest ecology, there’s also a cheerleading quality about it. I’ve done environmental impact work, and yes, you feel some pressure to look out for the interests of the people who are paying you. But it isn’t in anyone’s interest to produce a bad product. The “reforestation plan” (starts on p. 25) also seems awfully unrealistic.

Also:

• BirdLife International: Windfarm permit “seriously contradicts” Endangered Species Act.
• Online petition asking Puerto Rican Governor Aníbal Acevedo Vilá to protect the site.

More:

• Species-area curves – when they get the get the most basic biology so badly wrong, you tend to lose confidence in what they have to say rather rapidly.
• Puerto Rican nightjar, part I.