The Lives of Bees
Page 40
al. (2003) and Groh et al. (2004). Their findings show that this narrow range of temperatures is typical for the brood nests of honey bee colonies.
Page 217: At present, we lack good data on the thickness of the walls of natural tree cavities occupied by honey bees, and we do not know if wall thickness is assessed by scout bees when they are
inspecting prospective nest cavities. Fig. 5.1 shows the width of the walls of one natural nest cavity; the walls vary in width from ca. 8 cm to 13 cm (ca. 3 to 5 in.).
Page 217: The isotherm lines for the hive depicted in Fig. 9.1 are based on readings from 192 thermo-couples that were mounted in 12 horizontal rows in the central plane of the hive, between the two centermost frames of comb. The thickness of the hive’s wooden walls was 19 mm (0.75 in.).
Page 218: That the flight muscles of insects have some of the highest known levels of metabolic activity is discussed in Bartholomew (1981). The weight- specific rates of power output for a honey bee
come from Heinrich (1980) and for an Olympic rower come from Neville (1965). The efficiency
of the insect flight apparatus in converting fuel to mechanical power is discussed in Kammer and Heinrich (1978).
Page 219: For more information on how strongly bees can elevate their thorax temperature above
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ambient temperature, see Esch (1960) and Heinrich (1979b). The need of worker honey bees to
maintain thoracic temperature above about 27°C (81°F) is reported by Esch (1976) and Heinrich
(1979b), and is explained by Josephson (1981) and Heinrich (1977). The ability of worker honey
bees to warm their flight muscles through isometric contractions of these muscles is analyzed by Esch (1964).
Page 219: That honey bees use the same mechanism for warming their flight muscles and heating their nests is shown in Esch (1960). Bujok et al. (2002) and Kleinhenz et al. (2003) describe how a nurse bee can warm a pupa by pressing her thorax to a cell capping or by entering an empty cell adjacent to one containing a pupa and then producing heat with her flight muscles.
Page 221: That sustained brood- nest temperatures over 37°C (99°F) disrupt larval metamorphosis was shown by Himmer (1927). Chadwick (1931) reports that honey- laden combs will start to collapse
at 40°C (104°F). The upper lethal temperature for adult honey bees is reported by Allen (1959b)
and Free and Spencer- Booth (1962). That honey bees can survive several days at 15°C (59°F) was
shown by Free and Spencer- Booth (1960).
Pages 221–222: Vern G. Milum’s study of the effect of brood- nest temperature on worker development time is reported in his paper Milum (1930). Anna Maurizio’s study that found that a reduction to 30°C (86°F) for just a few hours is sufficient for a successful infection of larvae by chalkbrood fungus is reported in her landmark paper Maurizio (1934).
Page 222: The study that reports an elevated brood- nest temperature (fever) response to infection by the chalkbrood fungus, Ascosphaera apis, is reported in Starks et al. (2000).
Page 223: The work that found that bees chilled below about 18°C (64°F) cannot activate their flight muscles is Allen (1959b) and Esch and Bastian (1968). The study that showed worker bees enter a
chill coma when cooled below about 10°C (50°F) is that of Free and Spencer- Booth (1960).
Page 224: Conduction is the transfer of heat through a substance that is motionless. Convection is the transfer of heat through a substance by means of motion of the substance; it requires a flow of air or water. Evaporation of water takes heat away, because water absorbs considerable heat when it
changes from a liquid to a gas. Thermal radiation is heat transfer that occurs when an object emits electromagnetic radiation, such as infrared radiation.
Page 226: Detailed information about the temperature at which clustering starts is reported in Free and Spencer- Booth (1958), Kronenberg and Heller (1982), and Southwick (1982, 1985). Charles
D. Owens’s studies on the structure- temperature relations of colonies in winter are reported in Owens (1971). The statement that the volume of a colony’s cluster shrinks fivefold as the
temperature falls from 14°C to −10°C (57° and 14°F)—where the bees reach their lower limit of
cluster contraction—is based on fig. 22 in Owens (1971).
Page 227: The measurement of heat conductance from a 17,000 bee (ca. 2.2 kg/4.9 lb.) winter cluster of honey bees living in a Langstroth hive is reported in Southwick and Mugaas (1971). The similarity in heat conductance for an overwintering colony of bees and birds and mammals is shown in Fig. 5
of this paper.
Pages 227–229: The pioneering studies on the differences in heat conductance between the walls of natural tree cavities and various man- made hives and on the consequences of these differences are reported in Mitchell (2016, 2017).
Page 230: The two cavities have the same dimensions for width, depth, and height: 24 cm × 24 cm ×
87 cm (9.5 in. × 9.5 in. × 34 in.). The tree cavity was made by cutting into a sugar maple tree
whose diameter at the height of the cavity is 96 cm (37.8 in.), removing slices of wood, and
smoothing the inner surfaces with an adze. The walls around the cavity differ in thickness. The
thinnest is the removable front wall (with the entrance): 15 cm (6 in.). The thickest is the back wall: 57 cm (22.4 in.). Side walls are 36 cm (14.2 in.) thick. Temperature data are collected by an array Seeley.indb 309
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of Raspberry Pi microcontroller temperature sensor/recorder units mounted in each box and
powered by a solar panel in the tree.
Page 232: The figures for the pooled, resting metabolism of brood and adult bees at 35°C (95°F) come from Allen (1959b), Cahill and Lustick (1976), and Kronenberg and Heller (1982). The figure of
500 watts/kg (230 watts/lb.) for the maximum metabolic rate for honey bee flight muscle comes
from Jongbloed and Wiersma (1934), Bastian and Esch (1970), and Heinrich (1980).
Page 232: The study that revealed that a nurse bee will incubate pupal brood by heating her thorax and pressing it to the capping of a brood cell is Bujok et al. (2002).
Page 232: The strong increase in metabolic rate of small groups of bees—from ca. 30 watts/kg (13.5
watts/lb.) at 36°C (97°F) to ca. 300 watts/kg (135 watts/lb.) at 5°C (41°F)—to resist chilling was reported by Cahill and Lustick (1976).
Page 233: The plot of colony metabolic rate as a function of ambient temperature and cluster formation (Fig. 9.7) is from Southwick (1982).
Page 234: The experiment by Lindauer in Italy is described in his 1954 paper on the temperature
regulation and water economy of honey bee colonies; see Lindauer (1954).
Page 235: Two early reports that bees start fanning (for cooling) when the temperature inside the brood nest reaches 36°C (97°F) are Hess (1926) and Wohlgemuth (1957).
Page 235–236: The work by Jacob Peters and colleagues is reported in Peters et al. (2017). The reports by Engel H. Hazelhoff of honey bee nest ventilation for temperature control and carbon dioxide
removal are Hazelhoff (1941) and Hazelhoff (1954). An experimental study of nest ventilation in
response to high levels of carbon dioxide is Seeley (1974).
Page 236–237: The natural experiment in southern California that demonstrated the importance of
water for cooling honey bee colonies is described in Chadwick (1931).
Page 237: The evidence that some foraging- age bees specialize in water collection for days, if not weeks, comes from Lindauer (1954), Robinson et al. (1984), Kühnholz and Seeley (1997), and Ostwald
et al. (2016). The analysis of how water collectors fuel their flights home is found in Visscher, Crailsheim et al. (1996). The various purposes for which honey bee
s collect water are described in Park (1949), Nicolson (2009), and Human et al. (2006).
Page 238–239: The observations of water collection in winter by bees in northern Scotland are reported in Chilcott and Seeley (2018). The analysis, using an infrared camera, of the thermoregulation techniques of water collectors in winter is described in Kovac et al. (2010). For a detailed report on thermoregulation by water collectors—also investigated using an infrared camera—see
Schmaranzer (2000).
Page 239: To read Derek Mitchell’s analysis of the effects of top entrances on the temperature and humidity of colonies living in well- insulated hives, see Mitchell (2017).
Page 240: The studies of the activation and deactivation of the water collectors in a honey bee colony as it experiences a temporary heat stress are reported in Ostwald et al. (2016) and Kühnholz and Seeley (1997).
Page 242: The reports by beekeepers in Australia and South Africa of water storage in the combs are Rayment (1923) and Eksteen and Johannsmeier (1991). The report by O. Wallace Park of clusters
of reservoir bees filled with water is Park (1923).
CHAPTER 10. COLONY DEFENSE
Page 243: The Henry David Thoreau quotation is from his essay “Walking”; see Thoreau (1862), p. 665.
Page 243: For an extensive review of the several hundred organisms that will consume part or all of a honey bee colony if they can penetrate the bees’ defenses, see Morse and Flottum (1997).
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Page 244: The view that honey bees have a long evolutionary history with most of their infectious diseases, and that beekeepers sometimes seriously interfere with the bees’ natural mechanisms for controlling the agents of their diseases, is discussed in the authoritative books on honey bee pathol-ogy by Bailey (1963, 1981) and Bailey and Ball (1991).
Page 244–245: The history of the transport of colonies of European Apis mellifera from Ukraine to the Far East region of Russia is summarized in Crane (1999, pp. 366–367).
Page 245: High virulence is expected to evolve in pathogens and parasites that spread easily between genetically unrelated hosts (horizontally) rather than from parent to offspring (vertically). This is because the horizontal transmission of pathogens/parasites favors strains that reproduce vigorously, and this high reproduction generally harms the host. In contrast, vertical transmission favors
pathogens/parasites that reproduce slowly enough to leave the host healthy enough to produce the offspring that the pathogen or parasite needs for its next hosts. For a more detailed explanation of how the evolution of virulence depends on the ecology of the pathogen/parasite, see Ewald (1994, 1995). In honey bees, horizontal transmission (between unrelated colonies) of deformed wing virus (DWV) can occur in two ways: 1) when workers infested with Varroa mites carrying DWV drift into uninfested colonies, and 2) when workers rob a colony with Varroa mites carrying DWV and then bring these mites home.
Page 245: I have not been able to find reliable information on when Varroa mites began to infest colonies of Apis mellifera in the Primorsky region of Russia, but a report by Crane (1978) suggests that it occurred soon after peasants from Ukraine, who brought with them colonies of Apis mellifera, started settling in the region in 1883 (see Ihor Samokysh, Ukrainians in Zeleny Klyn, Day Kyiv, 17
November 2011, https://day.kyiv.ua/en/article/day-after-day/ukrainians-zeleny-klyn; accessed
28 June 2018).
Page 245: The studies of Martin (1998), Martin (2001), and Martin et al. (2012) have shown that the primary cause of the widespread mortality of honey bee ( Apis mellifera) colonies is coinfections of the bees by Varroa destructor and viruses, especially the deformed wing virus.
Page 246–247: The mechanisms of resistance to Varroa destructor by honey bees from far- eastern Russia were elucidated by a team of researchers working at the Honey Bee Breeding, Genetics, and
Physiology Research Laboratory of the U.S. Department of Agriculture, in Louisiana. Their detailed and multifaceted studies are reviewed in Rinderer, Harris et al. (2010). The detailed report of the controlled field study that demonstrated conclusively the genetically based resistance to Varroa destructor of the bees imported from far- eastern Russia is Rinderer, Guzman et al. (2001).
Pages 247–252: For detailed information about the design and results of the experiment that has
tracked an isolated, Varroa- infested population of honey bees living on the island of Gotland, Sweden, see Fries, Hansen et al. (2003), Fries, Imdorf et al. (2006), and Locke (2016). For
information about the mechanisms of Varroa- mite resistance of the Gotland bees, see Fries and Bommarco (2007), Locke and Fries (2011), Locke (2015, 2016), and Oddie, Büchler et al. (2018).
Page 252: The amazing skill of Varroa mites in climbing onto worker bees while they are foraging on flowers is described in Peck et al. (2016). This paper includes a link to a lovely video that shows the incredible nimbleness of these mites.
Page 253: The methods of bee hunting alluded to here are described in full in Seeley (2016).
Pages 253–254: For more information about the investigation of whether the honey bees living in the Arnot Forest are genetically distinct from the bees living in the apiaries nearest to this forest, see Seeley, Tarpy et al. (2015).
Page 254–257: The genetic study of the old (museum) and new (modern) samples of wild- colony bees, using whole- genome sequencing, is reported in Mikheyev et al. (2015).
Page 257: The reports of other collapses (but not extinctions) of populations of wild or abandoned Seeley.indb 311
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honey bee colonies after the arrival of Varroa destructor come from Texas, Arizona, Louisiana, Sweden, Norway, and France. See, Texas: Pinto et al. (2004); Arizona: Loper et al. (2006); Louisiana: Villa et al. (2008); Sweden: Fries, Imdorf et al. (2006), Norway: Oddie, Dahle et al. (2017), and France: Le Conte et al. (2007) and Kefuss et al. (2016).
Page 257–258: The work of David Peck is not yet published but will appear shortly in a paper titled
“Multiple mechanisms of behavioral resistance to an introduced parasite, Varroa destructor, in a survivor population of European honey bees.”
Page 258: The evidence that simply uncapping and recapping mite- infested cells of worker brood is an effective way for worker bees to reduce Varroa mite reproductive success (and does so without killing their worker brood) is reported in Oddie, Büchler et al. (2018).
Page 258–259: The history of the shift from bee hunting to beekeeping is described most fully by Crane (1999). For information on how colonies grouped in apiaries, relative to ones living in widely
dispersed nests, experience greater competition for forage, see Crane (1990, p. 194); experience higher risk of having honey stolen during nectar dearths, see Free (1954) and Downs and Ratnieks (2000); experience more problems in reproduction (especially queen loss), see Crane (1990, p. 196); and experience greater risk of acquiring disease, see Free (1958) and Goodwin and Van Eaton
(1999).
Pages 260: The figure of 40% or more bees drifting to a non- natal colony comes from Jay (1965, 1966a, 1966b). Studies of the effectiveness of various ways to reduce bee drift among colonies in apiaries are reported in Jay (1965, 1966a, 1966b) and Pfeiffer and Crailsheim (1998).
Pages 260–263: The experimental study that is described here, on the effects of crowding honey bee colonies in apiaries, is Seeley and Smith (2015). A related study, Frey and Rosenkranz (2014), has looked at how differences in colony spacing on the landscape scale (i.e., in regions with low vs. high colony densities) can also strongly affect the rate at which colonies acquire Varroa destructor mites from their neighbors in autumn.
Pages 263–268: The experimental study of the importance of small nests and frequent swarming in
helping wild colonies survive despite being infested with Varroa destructor is Loftus et al. (2016
).
Page 264–265: A study that shows that colonies living in small hives swarm more often than ones living in large hives is Simpson and Riedel (1963). A study that shows that approximately 50% of the mites in a colony are on the adult bees and 50% are in the sealed brood is Fuchs (1990).
Page 268: Donzé and Guerin (1997) provide a superb description of where and how immature Varroa destructor mites spend their time in the capped brood cells of honey bees. For a comprehensive description of the life cycle of Varroa destructor, see Rosenkranz et al. (2010). Among the first to suggest that smaller comb cells might cause higher mortality of immature Varroa mites were Erickson et al. (1990) and Medina and Martin (1999).
Page 269: The three previous tests of the idea of giving colonies of European honey bees combs of small cells to reduce their vulnerability to Varroa mites are Ellis et al. (2009), Berry et al. (2010), and Coffey et al. (2010). The test of this idea that I made with Sean Griffin is Seeley and Griffin (2011).
Page 270: The study by John McMullan and Mark J. F. Brown of the fill factor of brood combs with large and small cells is McMullan and Brown (2006).
Page 270: The study that shows the benefits to colonies of south- facing entrances is Szabo (1983a).
Page 273: My reference book on the mammals of eastern North America is Whitaker and Hamilton
(1998).
Page 273: Several important in vitro studies of the inhibitory effects of propolis on the growth of various bacterial and fungal pathogens of honey bees are Antúnez et al. (2008), Bastos et al. (2008), Bilikova et al. (2013), Lindenfelser (1968), and Wilson et al. (2015).
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Pages 274–276: The work from the laboratory of Marla Spivak that is summarized here is reported in two papers: Simone et al. (2009) and Borba et al. (2015). Another study that presents strong
evidence of the health benefits of propolis in the nests of honey bees—a strong correlation between the intensity of a colony’s propolis collection and its life span and brood viability—is Nicodemo et al. (2014).