Keith Delaplane 2016-09-08 12:16:11
Body Size in the Superorganism
I knew Bergmann’s rule before I’d even heard of it. And I bet most of my readers do too.
My epiphany came on one of my trips back home to Indiana after I had moved to Louisiana to go to school at LSU. It was my first trip back to Indiana during summertime, the previous trips having been limited to Christmas when the squirrels weren’t out. Squirrels, that is, because my epiphany had to do with squirrels, and summer-time because that meant it had been a long time since I’d been home. The first time I laid eyes on a Hoosier squirrel after years of absence I about jumped: they were so big they looked liked dachshunds running up the trees. It’s true. Indiana squirrels are bigger than Louisiana squirrels. And beekeepers who’ve had the opportunity to work bees in different parts of the country know that the same applies to honey bees as well: worker bees are bigger in Indiana than they are in Louisiana – or pretty much anywhere north versus south. Only later did I learn that this observation had been noted before: that animal body size increases as latitude increases. It can apply both within species and across species within a genus. It is general enough to be called a rule of biogeography, named after Carl Bergmann, the 19th C German biologist who first wrote about it in 1847.1 But it is far from universal, and in the case of insects may even be weak. Among the Hymenoptera, the order making up the ants, wasps, and bees, only 25 of 62 studies (40%) have confirmed Bergmann’s rule2, and among the bumble bees in particular the opposite seems to hold – that body size gets smaller as latitude increases (called “converse Bergmann”).3 I raise the issue at all because I think Bergmann’s rule has something to say in our evolutionary history of the honey bee, and what little information exists on the matter suggests that A. mellifera does indeed follow it.4
This month’s installment is about the evolution of body size in Apis mellifera, and in spite of my casual observation that worker bees are bigger in Indiana, readers of this column will know that a more insightful way to think about body size in the honey bee is to consider the superorganism – how many workers make up a colony? If it is true that a colony is analogous to a unitary, multi-cellular organism such as ourselves, then we can think about worker bees as cells of the body, and the more cells the bigger the body. Among members of its genus, A. mellifera has a relatively high worker population. A comparison of natural colony populations in the genus Apis is shown in the table along with other measures of interest, copied from Seeley5 and Dyer and Seeley.6
Colony population size is important for modern beekeeping, and by one’s first or second season a new beekeeper has learned to distinguish an unacceptably small population from a large one (Fig. 1). Basically, the more the better, and any deviation from this is a sign that something’s wrong. For example, Colony Collapse Disorder (CCD) is, by definition, a worker population proportionally small to the amount of brood.7
It was a USDA scientist, C.L. Farrar, who showed just how important large populations are to honey production. His landmark 1937 paper8 showed that honey hoarding efficiency increases as colony population increases. In other words, one colony of 50,000 bees can be expected to make more honey than the sum of two colonies of 25,000 bees. The historic importance of this discovery cannot be overstated, and I personally think C.L. Farrar has a claim to the beekeeping pantheon at least as great as our venerated L.L. Langstroth.
In one stroke, Farrar reinvented honey production management. Prior to Farrar, beekeepers were mostly concerned with large hive numbers. Swarms were considered a good thing as one now had two hives instead of one. The famous old beekeeping rhyme betrays this antiquarian point of view:
A swarm of bees in May is worth a ton of hay.
A swarm of bees in June is worth a silver spoon.
A swarm of bees in July ain’t even worth a fly.
Now I have to admit I’ve puzzled over the valuations used in this old ditty, so I went to Google and Amazon to enlighten me. A ton of alfalfa hay runs about $150- $250, and silver spoons from Amazon run about $86. But whether it’s May or June I think a new swarm would be hard-pressed to make anything close to that value in honey. After Farrar it was realized that swarming, by reducing a colony’s foraging force by half, is a severe blow to honey production, and today’s bee management is essentially the pursuit of very large colonies that don’t swarm. We can thank Farrar for feeding, reversing, splitting, combining, equalizing, cell-cutting, requeening, supering, and all the other things we do to prevent swarms and maximize colony size.
If large worker populations are good for the beekeeper, they’re also good for the superorganism, and today’s large worker populations in A. mellifera can be thought of as another optimized outcome of selection by natural forces. As we have seen in other characteristics of bees, colony population is a messy outcome of genetic evolution, physical constraints placed on the bee, and positive feedback loops that reinforce evolution of large populations.
To understand how this happened, we need to go back to the breeding ground of the genus Apis, Southeast Asia, and reconstruct the plausible pathways inferred from behaviors observable in modern species. Readers of this column will recall that modern Apis can be divided into two camps – those that nest on single open combs and those that nest on multiple combs in cavities. It has been resolved beyond reasonable doubt that the primitive condition is single open combs, and the later derived development is cavity nesting.9 All modern single open-comb nesters, of which A. florea and A. dorsata are represented in the table, express a primitive behavior unknown in the cavity nesters, represented in the table by A. cerana and A. mellifera. The open-nesters have a “curtain” of living bees that hangs over the comb covering the queen, the brood, and the nurse bees tending it (Fig. 2). This curtain provides a defensive barrier against enemies such as predatory hornets and a measure of temperature insulation. It mirrors the function of a physical shelter.
It is believed that the shift from open nesting to cavity nesting was a watershed moment in the evolution of Apis, beginning with the obsolescence of the living bee curtain. With the onset of cavity nesting, the worker cohorts formerly engaged passively as living insulation were now freed to contribute more directly to the economy of the colony.
The implications of this evolutionary fork in the road were hinted at by a pair of studies that compared metabolism and foraging rates of modern open nesters against cavity nesters.6,10 The authors, Fred Dyer and Tom Seeley, showed that cavity nesting species have a higher “tempo,” by which they meant metabolic rate and foraging rate. This pattern did not track with body size as one might expect – metabolism usually increases as body size gets smaller11 – because workers of the low-tempo open nesters included both the largest and smallest workers in the study, and workers of the two cavity nesters were intermediate (see table). Nesting habit, not body size, seems to be the unifying principle.
Combining Dyer and Seeley’s work with later studies enables us to reconstruct a chain of events by which cavity nesting led to characteristics familiar to the modern honey bee: (1) As workers were freed from passive curtain duty, more of them were available for nursing, foraging, and other tasks in support of brood; (2) as the colony’s foraging economy improved, this encouraged more brood rearing and the innovation of multiple combs to support it; (3) the increasing ratio of brood : workers had a stimulating effect on foraging12, thus increasing selection for high worker metabolism and productivity; (4) the positive feedbacks of more brood and increased foraging reinforced larger colony populations, and finally (5) larger worker populations had a stimulatory effect on worker division of labor and task specialization, further increasing colony efficiency, constituting yet more positive feedback loops toward large populations.
And in perhaps the biggest positive feedback loop of all – large populations are not only an outcome of complex eusocial colony life, but they seem necessary to complex eusocial life. I know this sounds like the chicken-or-egg paradox, but long-term readers of this column may remember in June 2015 when we talked about worker coercion – workers eating each other’s eggs – and how this behavior reinforces reproductive loyalty to the queen and promotes altruistic group living. In small populations it’s easy for one worker to physically dominate her sisters and insist on laying her own eggs, but this license fades away in larger populations where dominant wannabes have too many competitors. Large populations therefore have a selecting effect for social cohesion.13
With all these positive feedback loops one must wonder what prevented even larger worker populations than the 15,000-40,000 we see today – and the answer is seasonal and physical constraints imposed upon early Apis mellifera and its ancestors. First, the seasonal: for a vegetarian insect committed to living off stored nectar and pollen there is a finite periodicity to the availability of these resources. The few weeks of nectar flow in much of the temperate world are too brief to allow unlimited population growth. Second, the physical cavities: It seems to me that there is a finite range of cavity sizes that could meet the conditions necessary for the natural history I propose above: too small a cavity would not permit the extra combs and extra brood that initiate the positive feedback loops toward large populations; too large a cavity – a cave for example – would limit climate control and daytime flight orientation. Moreover, in the case of African and European A. mellifera that nest in hollow trees, there is a limit to the range of volumes available in tree hollows. A simple thought experiment shows us that an infinitely large hollow could only occur in a tree that was dead. It so happens that we know a little bit about the range of volumes available in tree hollows, and in the case of European bees in temperate latitudes that figure ranges between 15-80 liters5. I have always thought it was an interesting case of serendipity that L. L. Langstroth and his good friend A.I. Root settled on an American hive body volume of 50 liters which, with additional hive bodies and supers, generously accommodates the evolutionary constraint imposed upon Apis mellifera.
Not all cavity nester populations are equal. Our western honey bee, A. mellifera, has conspicuously larger populations than her tropical Asian cousin A. cerana (see table). This is where I believe Bergmann’s rule comes to play, bearing in mind that it is A. mellifera who pioneered into the temperate latitudes during her natural history. Bergmann’s explanation for larger body size at higher latitudes has to do with thermo-regulation, that larger bodies confer greater homeostasis and resistance to temperature extremes. This may be true. But alternative explanations are equally plausible, including the observation that larger body size permits a measure of buffering against food dearths. In mammals this means fat reserves, but in social insects this means stored food or cannibalized brood. In ants it has been shown that large colonies survive prolonged dearth better than small colonies.14 Bees also practice brood cannibalism when colonies are starving, and mangled pupae outside the hive entrance is a sure sign the beekeeper needs to step in with emergency feed.
And finally, we should note that the colony populations we’ve been talking about are colony populations in nature. In managed colonies it’s not uncommon for populations to achieve 50,000-60,000 bees or even higher. This is an outcome of generous hive volumes, courtesy of Langstroth and Root, and the swarm-prevention management practices precipitated by C.L. Farrar. In this, modern beekeeping is in step with all other sectors of agriculture – a human enterprise of coaxing levels of productivity in plants and animals far in excess of their natural optima for survival. Whether this is a good thing or not is an important question that invites reflection on the kind of production paradigms we modern humans have created. Whether these paradigms can be sustained and optimized for the general good of humans and the environment upon which we depend will be among the most important questions facing the next generations.
But for our present purposes, colony population – the size of the superorganism – is both a definitive characteristic of the honey bee and an explanation for beekeeping as we know it. Commercial-scale honey production and levels of honey consumption known now and throughout human history would never have been achieved if honey had remained a feature of small, wild bee nests. It would have been the stuff of hunting and gathering, not agriculture.
References
1 Bergmann, C. 1847. Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Studien 3(1): 595-708
2 Shelomi, M. 2012. Where are we now? Bergmann’s rule sensu lato in insects. The American Naturalist 180(4): 511- 519
3 Ramírez-Delgado, V.H. et al. 2016. The converse to Bergmann’s rule in bumblebees, a phylogenetic approach. Ecology and Evolution doi:10.1002/ ece3.2321
4 Ruttner, F. et al. 2000. Ecoclines in the Near East along 36° N latitude in Apis mellifera L. Apidologie 31: 157-165
5 Seeley, T.D. 1985. Honeybee ecology: a study of adaptation in social life, Princeton University Press
6 Dyer, F.C. and T.D. Seeley. 1987. Interspecific comparisons of endothermy in honey-bees (Apis): deviations from the expected size-related patterns. Journal of Experimental Biology 127: 1-26
7 vanEngelsdorp D. et al. 2009. Colony Collapse Disorder: A descriptive study. PloS ONE 4(8): e6481. Doi:10.1371/ journal.pone.0006481
8 Farrar, C.L. 1937. The influence of colony populations on honey production. Journal of Agricultural Science 54: 945- 954
9 Raffiudin, R. and R.H. Crozier. 2007. Phylogenetic analysis of honey bee behavioral evolution. Molecular Phylogenetics and Evolution 43: 543-552
10 Dyer, F.C. and T.D. Seeley. 1991. Nesting behavior and the evolution of worker tempo in four honey bee species. Ecology 72: 156-170
11 Calder, W.A. 1984. Size, function, and life history. Harvard University Press, Cambridge, Massachusetts, USA.
12 Pankiw, T. et al. 1998. Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behavioral Ecology and Sociobiology 44: 193-198
13 Bourke, A.F.G. 1999. Colony size, social complexity and reproductive conflict in social insects. Journal of Evolutionary Biology 12: 245-257
14 Kaspari, M. and E.L. Vargo. 1995. Colony size as a buffer against seasonality: Bergmann’s rule in social insects. The American Naturalist 145: 610-632
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