The species-area relationship and Bergmann’s rule: attempts to explain global patterns in biodiversity

Introduction

Humans have noticed the differences between species worldwide from the time they evolved up until the present, with the term “biodiversity” first being used by Tangley (1985). A natural progression from these discoveries of global biodiversity was to explain them using such rules as the species-area relationship (SAR) and Bergmann’s rule. SARs describe the link between the area of a habitat and the number of species found within that area (Losos & Schulter, 2000; Preston, 1962). Bergmann’s rule states that species of larger size are found in colder regions, and species of smaller size are found in warmer regions (Ashton, Tracey, & de Queiroz, 2000; Mayr, 1956). Both rules are utilised in the field of biogeography, and I will be looking at evidence that both supports and opposes SARs and Bergmann’s rule to critique the validity of each.

The SAR model has ideas such as island biogeography theory (IBT) and spatial scales and studies that support it as an ecological law (Franzén, Scweiger, & Betzholtz, 2012; Losos, 1996; Losos & Schluter, 2000; Rand, 1969). IBT states that larger islands have greater numbers of species than smaller islands (MacArthur & Wilson, 2001; MacGuinness, 1984) and spatial scales keeps each SAR study relevant to the size at which the study was undertaken (Drakare, Lennon, & Hillebrand, 2006; Turner, 2005; Tylianakis, Klein, Lozada, & Tscharntke, 2006). Criticism of IBT says that its equilibrium theory is too simplistic, which raises questions about it being successfully used to support SARs (Heaney, 2000; Lomolino, 2000; Tangney, Wilson, & Mark, 1990; Toft & Schoener, 1983; Webb & Vermaat, 1990; Wu, 1995). A lack of real-life SAR studies poses the question: is SARs more valuable as a tool for biogeography rather than an ecological rule (Diamond, 1984; Zimmerman, 2000)? 

Bergmann’s rule is supported by real-life studies that not only expressed the rule but followed a logical reason as to why they adhered to it (Ashton, Tracy, & de Queiroz, 2000; Fujita, 1986; Gigliotti et al., 2019; James, 1983; Rhymer, 1992; Sand, Cederlund, & Danell, 1995; Weaver & Ingram, 1969). Conversely, there are some exceptions to Bergmann’s rule that also carry their own rational explanation (Gigliotti et al., 2019; Oishi, 2010; Takeuchi, 1995; Kaneko, 1988). Geist (1987, 1990) disagrees with Bergmann’s rule and pointed out that not only is body mass a poor conserver of heat, but that body size is also due to a multitude of different factors. 

Species-area relationship

Supportive evidence for species-area relationship

SARs depict the number of species found in an area of habitat and are plotted on a graph to show a species-area curve where x = habitat area and y = species richness (Rosenzweig, 1995). The typical outcome of plotting SARs on a graph is a sharp increase in species richness over the initial area that begins to taper off as distance increases; it shows that, over a habitat area, species richness increases. Franzén et al. (2012) regarded SARs as an ecological tool used to make predictions for areas that have little or no data behind them. This means SAR predictions can be used as a powerful instrument in conservation for remote habitats or when there is little time to collect data in the field. 

The theory of island biogeography was coined by MacArthur and Wilson in 1967, and it states that species richness increases with island size and decreases with island distance from the mainland (MacArthur & Wilson, 2001). These islands receive new colonising species from the mainland, and, eventually, established populations of species become extinct; this creates an equilibrium point where immigration equals extinction. A study by Riebesell (1982) found that the species richness of plants on 13 peaks in the Adirondack Mountains is due to the area of the alpine ecosystem and immigration between summits. This reflects IBT as the plant seeds have been spread by birds and dropped on mountaintops (more seeds dropped on a bigger area). Extinction was evident because the plants on the island were not genetically identified as relict populations, meaning that an equilibrium has been met between seed dispersal (immigration) and plants dying (extinction). 

Spatial scales are essential in verifying the use of SARs in the context of the study being undertaken (C. Bishop, personal communications, May 7, 2020). This amplifies SAR effectiveness because it gives a guideline as to how SARs should be studied and therefore reduces the likelihood of error; when spatial scales are considered during SAR research, it increases the integrity of the research. Turner and Tjørve (2005) discuss spatial bias, where smaller areas are likely to be surveyed more intensely than larger ones for practical reasons, meaning that the number of species being sampled can potentially decrease with an increase in area. In a scenario such as this, the data will less likely represent the actual species richness of the area, reducing the validity of the species-area rule. A study of anthropogenic influences on bees and wasps by Tylianakis et al. (2006) found that estimation of species diversity of a larger area based on evidence gathered at a smaller spatial scale underestimated the actual result; had this gone unnoticed, it would have meant that greater conservation attention would have been given to the wrong area. This verifies the importance of using spatial scales to enhance SARs’ effectiveness.

Studies, such as those undertaken by Losos (1996) of the Anolis lizard and Franzén et al. (2012) of butterflies and moths on true islands show SARs as real examples. Losos (1996) found in his study of Anolis lizards on 147 Caribbean islands that a significant relationship exists between the number of species and area of the island. Larger islands were found to have more species present than smaller islands that were more geographically isolated and did not support more than 2 Anolis species at a time. This supports IBT and shows that Anolis lizards on smaller, more isolated islands have reached an equilibrium point, such as the one discussed by MacArthur and Wilson (2001). A positive relationship between area and species richness of 1016 moth and butterfly species was recorded by Franzén et al. (2012), who also noted species with a smaller geographic range were more sensitive to area change than species with a larger range; this emphasises the importance of spatial scales within SAR studies.

Counter-evidence for species-area relationship

There is a discussion about MacArthur and Wilson’s (2001) IBT to be used as more of a framework than a theory. It needs to be modernised, especially as its equilibrium model appears too simplistic (Heaney, 2000; Lomolino, 2000). As IBT is a SAR, any fragility found within IBT raises questions about the reliability of SARs as a law. IBT’s equilibrium model’s simplicity lies in the fact that it only accounts for species richness due to immigration and extinction and no other factors. Even so, the idea of equilibrium being reached on an island seems far-fetched as ecological stochasticity and geographical and geological fluctuations can affect a perfectly balanced model. Tangney et al. (1990) listed five other possible explanations for any studies that showed results consistent with IBT. These include random placement hypothesis (Arrhenius, 1921), habitat diversity hypothesis (Williams, 1943), incidence function hypothesis (Diamond, 1975), small island effect hypothesis (Whitehead & Jones, 1969), and small island habitat hypothesis (Kelly, Wilson, & Mark, 1989).

Assumptions of IBT (MacArthur & Wilson, 2001), and therefore SARs, can be challenged:

  1. Species richness balances immigration rates and extinction rates, excluding speciation over evolutionary time. For example, the adaptive radiation resulting in different finch species on the Galapagos Islands (Grant & Grant, 2008).
  2. The assumption that immigration rates to an island result from island size and distance from the mainland fail to account for other variables. These variables include the role ocean and air currents play in transporting species to islands (Payn, Dvorak, & Myburg, 2007), anthropogenic introduction of species, or immigration from other islands or emigration from the island.
  3. IBT ignores stochastic events and assumes that all species have an equal ability to immigrate or become extinct.
  4. Natural disasters can cause extinction on islands; natural disasters can also function independently of island size or distance to the mainland. 
  5. Climate can affect the species’ likelihood to immigrate to or leave an island. For example, a species that functions in colder weather on the mainland is unlikely to leave its niche to travel to a warmer island, and vice versa, regardless of the islands size or proximity to the mainland.

As mentioned before, SAR’s equations and models are used in conservation. Still, Zimmerman and Bierregaard (1986) introduce the thought of SAR data acting as a “blindman’s cane [to] show us roughly the way” (p. 141) after stating that predictions using IBT and SARs for conservation were nonbeneficial. Diamond (1984) mentions that the speed at which environments are being dismantled should cause ecologists to erect conservation plans faster for them to be preserved. A study of Amazonian frog conservation (Zimmerman and Bierregaard, 1986) was used as a case for the misuse of SARs and IBT and showed that these models may underestimate species richness. Therefore, mean areas receive less conservation than they need. Zimmerman and Bierregaard (1986) propose that time spent studying theory would be better used to understand the relationships that species have with their environment, which would, in turn, produce a better estimate of species richness in an area than using SAR equations. There were many articles available on SARs, yet it was all theory with little in-field evidence; lack of evidence challenges the integrity of the law. The questions here are: is the SAR model an excuse to use maths and models instead of physical evidence which could say otherwise? Is there too much theory and not enough tested hypotheses? Is the consequence of a lack of conservation, where it is needed, taxonomic extinction? In-field experimentation is necessary to answer these questions.

Bergmann’s rule

Supportive evidence for Bergmann’s rule

Bergmann’s rule says species of larger size are found in colder environments, whilst their smaller counterparts are found in warmer environments (Ashton, Tracey, & de Queiroz, 2000; Mayr, 1956). Many arguments have arisen about the validity of Bergmann’s rule (Geist, 1987, 1991; Paterson, 1990), yet, animals are not set aside from the laws of physics (Cambell, 1977), and Paterson (1988) states that Bergmann’s rule obeys mass and surface-area heat-transfer rules. (It is important to note that this refers to their mass or surface area when referring to smaller and larger individuals, rather than length unless noted (Paterson, 1988).)

Evidence of geographic variation in body size of birds has a solid environmental link, including that of the mallard ducks (Anas platyrhynchos) of America and Canada (Rhymer, 1992). It was found that the growth of the mallard ducklings was constrained by environmental conditions experienced during development; tarsus length was 3% longer in the colder Canadian population, and it was shown that this variation was due to the environment they were exposed to during maturation. James (1983) conducted a study with 12 avian species in the central and eastern United States. He found intraspecific size variation is related to a combination of temperature, moisture, and other climatic variables, rather than just temperate ones. A modification of Bergmann’s rule to include this will maintain the integrity and framework of the rule whilst adding more information and specificity to it.

Mammals in both controlled and natural environments displayed evidence of adhering to Bergmann’s rule. Pigs (Sus scrofa domesticus) raised at 5oC were bigger than pigs of the same species raised at 35oC (Weaver & Ingram, 1969). Swedish moose (Alces alces) not only had a 15-20% larger body mass in colder, northern areas than in the south, but also had higher growth rates and matured later than in warmer areas (Sand et al., 1995), indicating a slower metabolic rate for moose in colder environments. Bats (Myotic lucifugus) also showed a similar metabolic correlation to latitude and conforming to Bergmann’s rule in that the colder population grew slower, showed delayed aviation development, and were born larger (Fujita, 1986).

Northern American populations of snowshoe hare (Lepus americanus) conform to Bergmann’s rule to mitigate heat loss (Gigliotti et al., 2019). They can withstand the colder winter months by conserving heat and energy due to increased body mass. The strong selection pressure for larger female snowshoe hares is because females have higher energy demands due to gestation and lactation; the hares breed in winter months, so conserving energy during the cold period whilst also having maternal demands is essential for the hare. 

Counter evidence for Bergmann’s rule 

Contrarily, southern American snowshoe hare populations do not follow Bergmann’s rule as strongly as their northern counterparts (Gigliotti et al., 2019). This is an example of different selection forces acting on individuals, even within a species. In the northern population, a big driver for body mass was to conserve energy and mitigate heat loss, whilst, in the southern population, their large body mass was a result of an extended growing season. Gigliotti et al. (2019) found that the milder, southern winter meant heat conservation wasn’t an essential factor in determining hare body mass. Furthermore, southern populations experienced a long summer growing season and a shorter winter, meaning they had more time to accumulate body mass and less time to lose it.

Two subspecies of red fox (Vulpes vulpes) in Japan show a negative correlation to Bergmann’s rule as skull size is bigger in the subspecies inhabiting the warmer, southern regions than the subspecies inhabiting the colder, northern region (Oishi, 2010; Takeuchi, 1995). Oishi (2010) found the southern subspecies showed increasing skull size with decreasing latitude across its populations. Although the body length of the northern subspecies was larger than the southern subspecies, the male body weight was the same between both, and the female body weight was lighter in the northern species, countering Bergmann’s rule as colder populations had less body mass.

Geist (1987, 1990) opposes Bergmann’s rule with solid reasoning. Firstly, because Bergmann’s (1847) article is written in German, translation has become an issue, with many people following Mayr’s (1956) translation, which Geist (1989) claims is wrong. Secondly, using formulas derived from Bergmann’s rule, Geist (1987, 1990) predicts an exponential size increase with latitude, anticipating higher latitudinal populations of Calgarian sparrows to be the size of chickens, which they are not. Thirdly, Geist (1987) concludes that hair is a superior adaption than size to cold, predicting a hairless beast at different temperate intervals would finally have to weigh 15,000kg at a temperature of –32oC, whereas, for the same beast, 1cm of hair coat is worth a 5-fold increase in mass. Consequently, if it is cheaper to evolve a denser coat, evolution would favour this over body mass increase when subjected to cold stress. Finally, Geist (1990) concludes that body size depends not only on heat retention but also on other factors. These include: individuals surviving longer on larger fat stores; larger females bearing more and producing larger young; larger females producer richer or more milk, therefore sustaining healthier or more young respectively; large size favouring males in fighting and sexual selection; larger individuals can run for more extended periods (helpful in prey species were speed and endurance are necessary for survival). When considering these, it seems far-fetched that body size is solely due to selection for heat conservation at any latitude.    

Significance of ideas

In biogeography, it is essential to scrutinise these rules because it not only helps argue their place in science but uncovers more and more about the distribution of species in space and time. For SARs, it seems that more real-life evidence is needed to properly analyse this rule. For now, caution should be exercised when using it as a conservation tool. For Bergmann’s rule, it is clear there is a difference between and amongst species of different latitudes. Yet, it is naive and bold to assume these differences come down to something as simple as energy conservation. It seems far-fetched that Bergmann’s rule will hold true to species worldwide when you take in the complexities and specialised adaptations of the natural world.

I believe it is a scientist’s job to doubt rules (if only to end up strengthening their integrity in the end). Both SARs and Bergmann’s rule are a stepping-stone to the truth that nature hides. Any disparities should be indications of necessary modifications rather than a chance to disregard the rule entirely. 


References

Aho, J. (1978). Freshwater snail populations and the equilibrium theory of island biogeography. I. a case study in southern Finland. Annales Zoologici Fennici, 15, 146–154.

Arrhenius, O. (1921). Species and area. Journal of Ecology, 9, 95–99.

Ashton, K. G., Tracy, M. C., & de Queiroz, A. (2000). Is Bergmann’s rule valid for mammals?. The American Naturalist, 156(4), 390–415. 

Ashton, K. G. (2001). Are ecological and evolutionary rules being dismissed prematurely? Diversity and Distributions, 7(6), 289–295.  

Bergmann, C. (1847). Über die verhältnisse der wärmeökonomie der thiere zu ihrer größe. Goettinger: Vandenhoeck & Ruprecht

Campbell, G. S. (1977). An introduction to Environmental Biophysics. New York, New York: Springer-Verlag New York.

Diamond, J. M. (1975). Assembly of species communities. In M. L. Cody and J. M. Diamond (Ed.), Ecology and Evolution of Communities (pp. 342–444). Harvard University Press, Cambridge, Massachusetts, USA.

Diamond, J. M. (1984). Distributions of New Zealand birds on real and virtual islands. New Zealand Journal of Ecology, 7, 37–55. doi:10.1371/journal.pone.0037359 

Drakare, S., Lennon, J. J., & Hillebrand, H. (2006). The imprint of the geographical, evolutionary and ecological context on species-area relationships. Ecology Letters, 9, 215–227. doi: 10.1111/j.1461-0248.2005.00848.x

Fujita, M. S. (1986). A latitudinal comparison of growth and development in the little brown bat, Myotis lucifugus, with implications for geographic variation in adult morphology. Ph.D diss. Boston University, Boston. 

Franzén, M., Schweiger, O., & Betzholtz, P. E. (2012). Species-area relationships are controlled by species traits. PLoS ONE, 7(5):e37359. doi:10.1371/journal.pone.0037359  

Geist, V. (1987). Bergmann’s rule is invalid. Canadian Journal of Zoology, 65(4), 1035–1038. 

Geist, V. (1990). Bergmann’s rule is invalid: a reply to J. D. Paterson. Canadian Journal of Zoology, 68(7), 1613–1615. 

Gigliotti, L. C., Berg, N. D., Boonstra, R., Cleveland, S. M., Diefenbach, D. R., Gese, E. M., … Sheriff, M. J. (2019). Latitudinal variation in snowshoe hare (Lepus americanus) body mass: a test of Bergmann’s rule. Canadian Journal of Zoology, 98(4), 88–95. 

Gilbert, F. S. (1980). The equilibrium theory of island biogeography: fact or fiction? Journal of Biogeography, 7(3), 209–235. 

Grant, P. R., & Grant, B. R. (2008). How and why species multiply: the radiation of Darwin’s finches. Princeton University Press.

Hanski, I. (1981). Coexistence of competitors in patch environment with and without predation. Oikos, 37(3), 306–312. 

Heaney, L. R. (2000). Dynamic disequilibrium: a long-term, large scale perspective on the equilibrium model of island biogeography. Global Ecology and Biogeography, 9, 59–74. 

James, F. C. (1970). Geographic size variation in birds and its relationship to climate. Ecology, 51, 365–390. 

Johnson, K. P., Adler, F. R., & Cherry, J. L. (2000). Genetic and phylogenetic consequences of island biogeography. Evolution, 54(2), 387–396. 

Kaneko, Y. (1988). Relationship of skull dimensions with latitude in the Japanese field vole. Acta Theriologica, 33(3), 35–46. 

Kelly, B. J., Wilson, J. B., & Mark, A. F. (1989). Causes of the species-area relation: a sttudy of islands in Lake Manaouri, New Zealand. Journal of Ecology, 77, 1020–1028

Lloyd-Jones, L. R., Wang, Y., Courtney, A. J., Prosser, A. J., & Montgomery, S. S. (2012). Latitudinal and seasonal effects on growth of the Australian eastern king prawn (Melicertus plebejus). Canadian Journal of Fisheries and Aquatic Sciences, 69(9), 1525–1538. 

Lomolino, M. V. (2000). A call for a new paradigm of island biogeography. Global Ecology and Biogeography, 9, 1-6. 

Losos, J. B. (1996). Ecological and evolutionary determinants of the species-area relation in the Carribean anoline lizards. Philosophical Transactions of the Royal Society of London B, 351, 847–854. 

Losos, J. B. & Schluter, D. (2000) Analysis of an evolutionary species-area relationship. Nature, 408, 847–850. 

MacArthur, R. H., & Wilson, E. O. (2001). The Theory of Island Biogeography. Princeton, New Jersey: Princeton University Press. 

Mayr, E. (1956). Geographical character gradients and climatic adaptation. Evolution, 10(1), 105–108. 

McGuinness, K. A. (1984). Species-area curves. Biological Reviews, 59(3), 423–440. 

McNab, B. K. (1971). On the ecological significance of Bergmann’s rule. Ecology, 52(5), 845–854. 

Meiri, S., & Dayan, T. (2003). On the validity of Bergmann’s rule. Journal of Biogeography, 30(3), 331–351. 

Oishi, T., Uraguchi, K., Abramov, A. V., & Masuda, R. (2010). Geographical variation of the skull in the red foc Vulpes vulpes on the Japanese islands: an exception to Bergmann’s rule. Zoological Science, 27(12), 939–945. 

Paterson, J. D. (1990). Comment – Bergmann’s rule is invalid: a reply to V. Geist. Canadian Journal of Zoology, 68(7), 1610–1612. 

Payn, K. G., Dvorak, W. S., & Myburg, A. A. (2007). Chloroplast DNA phylogeography reveals the island colonisation route of Eucalyptus urophylla (Myrtaceae). Australian Journal of Biology, 55, 673–683. DOI: 10.1071/BT07056.

Powell, K. I., Chase, J. A., & Knight, T. M. (2013). Invasive plants have scale-dependant effects on diversity by altering species-area relationships. Science 339(6117), 316–318. 

Preston, F. W. (1962). The canonical distribution of commonness and rarity: part I. Ecology, 43, 185–215 + 410–432.

Rand, A. S. (1969). Competitive exclusion among anoles (Sauria: Iguanidae) on small islands in the West Indies. Breviora, 319, 1–16. 

Rhymer, J. M. (1992). An experimental study of geographic variation in avian growth and development. Journal of Evolutionary Biology, 5, 289–306. 

Riebesell, J. F. (1982). Arctic-alpine plants on mountaintops: agreement with island biogeography theory. The American Naturalist, 119(5), 657–674. 

Rosenzweig, M. (1995). Species Diversity in Space and Time. Cambridge, United Kingdom: Cambridge University Press.

Sand, H., Cederlund, G., & Danell, K. (1995). Geographical and latitudinal variation in growth patterns and adult size of Swedish moose (Alces alces). Oecologia, 102, 433–442.

Takeuchi, M. (1995). Morphological and ecological study of the red fox Vulpes vulpes in Tochigi, central Japan: a biological monograph on morphology, age structure, sex ration, mortality, population density, diet, daily activity patter, and home range use. PhD Thesis, Graduate school of Natural Science and Technology, Kanagawa University. 

Tangley, L. (1985). A new plan to conserve the earth’s biota. BioScience, 35(6), 334–336.

Tangney, R. S., Wilson, J. B., & Mark, A. F. (1990). Bryophyte island biogeography: a study in Lake Manapouri, New Zealand. Oikos, 59, 21–26. 

Toft, C. A., & Schoener, T. W. (1983). Abundance and diversity of orb spiders on 106 Bahamian islands: biogeography at an intermediate trophic level. Oikos, 41(3), 411–426. 

Turner, W. R., Tjørve, E., & Hillerbrand, H. (2005). Scale-dependance in species-area relationships. Ecography, 28(6), 721–730. 

Tylianakis, J. M., Klein, A. M., Lozada, T., & Tscharntke, T. (2006). Spatial scale of observation affects α, β and γ diversity of cavity-nesting bees and wasps across a tropical land-use gradient. Journal of Biogeography, 33, 1295–1304. doi:10.1111/j.1365-2699.2006.01493.x 

Weaver, M. E., & Ingram, D. L. (1969). Morphological changes in swine associated with environmental temperature. Ecology, 50, 710–713. 

Webb, N. R., & Vermaat, A. H. (1990). Changes in vegetational diversity on remnant heathland fragments. Biological Conservation, 53, 256–264. 

Whitehead, D. R., & Jones, C. E. (1969). Small islands and the equilibrium theory of insular biogeography. Evolution, 23, 171–179.

Whittaker, R. J., Fernández-Palacios, J. M., Matthews, T. J., Borregaard, M. K., & Triantis, K. A. (2017). Island biogeography: taking the long view of nature’s laboratories. Science, 357(6354):eaam8326. 

Williams, C. B. (1943). Area and number of species. Nature, 152, 264–267.

Wu, J., & Vankat, J. L. (1995). Island biogeography: theory and applications. Encyclopedia of Environmental Biology, 2, 371–379. 

Zimmerman, B. L., & Bierregaard, R. O. (1986). Relevance of the equilibrium theory of island biogeography and species-area relations to conservation with a case from Amazonia. Journal of Biogeography, 13(2), 133–143.