Temperature-dependent oxygen limitation in insect eggs
Section of Integrative Biology, University of Texas at Austin, Austin, TX 78712, USA
* Author for correspondence (e-mail: art.woods{at}mail.utexas.edu)
Accepted 18 March 2004
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Summary |
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Key words: moth, Manduca sexta, egg, oxygen availability, temperature, metabolism, eggshell, insect gigantism, Paleozoic hyperoxia
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Introduction |
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In insects, the importance of such interactions is less clear. Two older
studies demonstrated them (von Buddenbrock
and von Rohr, 1923; Keister
and Buck, 1961
), and, more recently, Harrison and Lighton
(1998
) showed that flying
dragonflies Erythemis simplicicollis, with thoracic temperatures of
about 40°C, released more CO2 in hyperoxia (30 and 50 kPa) and
less CO2 in moderate hypoxia (10 kPa). In addition, Frazier et al.
(2001
) showed that survival
and growth of Drosophila melanogaster (from egg to adult) were more
sensitive to oxygen availability at higher temperatures.
Here we examine temperatureoxygen interactions in eggs of a
terrestrial insect, Manduca sexta (Lepidoptera: Sphingidae). Because
of their small size and lack of mobility, terrestrial insect eggs often
experience large, rapid fluctuations in temperature. Eggs of M.
sexta, in particular, are common throughout temperate North America (see
Ferguson et al., 1999),
especially in the Sonoran and Mojave deserts where temperatures vary
substantially from day to night. Small size would seem to minimize problems of
oxygen transport. However, terrestrial eggs must also restrict water efflux
and prevent attack by predators and parasitoids, and doing so requires
elaborate eggshell layers (Hinton,
1981
) that may also restrict oxygen influx
(Tuft, 1950
;
Hinton, 1953
; Zeh et al.,
1988; Daniel and Smith, 1994
).
Such a set of tradeoffs appears to have driven the evolution of egg brooding
in the Belostomatidae; males in the subfamily Belostomatinae allow females to
lay eggs on their backs, which they then position at the airwater
interface and may actively ventilate when underwater
(Smith, 1997
). Although the
morphology of insect eggs and their eggshells is well known
(Hinton, 1981
;
Margaritis, 1985
; eggshell of
M. sexta: Orfanidou et al.,
1992
), little is known about egg metabolism and oxygen flux to
embryos. The only recent physiological work, by Daniel and Smith
(1994
), shows that size and
shape of the single aeropyle in eggs of Callosobruchus maculatus are
correlated with metabolic rate between strains. Understanding the effect of
temperature on oxygen supply and demand may provide insight both into
evolutionary constraints and pressures operating on eggshell design and, more
generally, into factors influencing the abundance and distribution of
insects.
Our ideas about temperatureoxygen interactions are guided by two
observations. First, insect embryos obtain oxygen by diffusion across their
eggshells (Hinton, 1981).
Second, oxygen supply by diffusion usually is less sensitive to temperature
than is oxygen demand by metabolic reactions. The latter relationship reflects
a more general principle that has been known for the past century: chemical
reactions are, in general, more sensitive to temperature than are physical
processes such as diffusion or electrical conductivity (Snyder,
1908
,
1911
;
Belehrádek, 1935
;
Sidell and Hazel, 1987
). The
consequence is that individuals obtaining oxygen by diffusion should, all else
being equal, experience oxygen limitation at high temperatures and surplus at
low temperatures (von Bertalanffy,
1960
; Bradford,
1990
; Atkinson and Sibly,
1997
; Woods,
1999
). This scenario is related to Pörtner's ideas about
oxygen supply and demand (Pörtner,
2001
,
2002
) but invokes a
different transport mechanism and predicts monotonically decreasing tissue
oxygen levels with increasing temperature. Evidence for temperature-induced
oxygen limitation in eggs is available primarily from studies of fish eggs
(Hamor and Garside, 1976
;
Czerkies et al., 2001
).
Bradford (1990
) also showed, in
a large comparative study of amphibians, that egg volume among species was
inversely related to incubation temperature, and he hypothesized that large
eggs may be oxygen limited at high temperatures. In addition, the oxygen
conductance of amphibian eggs increases during development as metabolic rate
increases (Seymour and Bradford,
1987
; Seymour et al.,
1991
) and, in some species, increases in response to environmental
hypoxia (Mills et al.,
2001
).
Our study focuses on two primary questions: Are insect embryos limited by oxygen availability? If so, is limitation more severe at higher temperatures? We use video-microscopy to measure survival rates and development times in eggs exposed to different combinations of temperature and oxygen. We then present data on metabolic rates (measured as CO2 emission rates) of eggs exposed to different oxygen levels and either steady or variable temperatures. Finally, using an oxygen microelectrode, we measure radial oxygen profiles in living and dead eggs at cool or warm temperatures. The results suggest that metabolism and development of eggs of M. sexta are oxygen limited, especially at high temperatures. Among insects the structure of Manduca eggs is unexceptional, implying that oxygen limitation of insect embryos may be widespread.
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Materials and methods |
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Survival and development times
Survival and development times from oviposition to hatching were measured
by video-microscopy in a 3x8 factorial experiment (three temperatures:
22, 27 and 32°C; eight O2 partial pressures: 9, 11, 13, 15, 17,
19, 21 (normoxia), and 30 kPa, with N2 making up the balance).
Oviposition times were determined to within 1 h by introducing potted tobacco
plants into the adult flight cage and removing them 1 h later. Eggs were
stripped from the leaves, weighed individually (to ±1 µg) on a
microbalance (Sartorius MC-5, Goettingen, Germany), and randomly assigned to
positions in one of three Plexiglas blocks (11.5 cmx12.5 cmx2 cm;
custom built by the Department of Chemistry's Machine Shop at the University
of Texas, USA). Each block contained eight cartridges that, in turn, each
contained 10 individual wells backed by Nitex mesh. Eggs were placed one to a
well (80 eggs per block; 240 eggs in total). With cartridges fixed into the
blocks, the wells isolated each egg and hatchling larva from other individuals
but exposed all ten eggs to the experimental gas flowing beneath the Nitex
mesh. The blocks were placed in incubators set to 22, 27 and 32°C.
Gases were handled with Bev-A-Line IV tubing (Cole Parmer, Vernon Hills, IL, USA). A preliminary experiment showed that eggs fared poorly in the dry air streams coming directly from gas cylinders. Therefore, upstream of the blocks, gas streams were bubbled through 100 ml distilled water in 250 ml flasks submerged in controlled-temperature baths. Bath temperatures were set so that the water-saturated gases emerging from the flasks would, once warmed to the experimental temperature, impose a uniform vapor density gradient of 10 g m3 (1.3 kPa) across the eggshells. Thus, for example, the streams going into the 27°C incubator (saturating vapor density 25.8 g m3) were bubbled through water at 18.4°C (saturated vapor density 15.8 g m3). Water baths for the 22 and 32°C incubators were set at 10 and 25.5°C, respectively. Because the latter was above room temperature, which would cause condensation in the lines, it was housed inside the 32°C incubator. This design avoids confounding effects of different vapor pressure gradients across temperature treatments. Gases, flowing at 100 ml min1 (checked daily with a bubble flow meter), were directed into each incubator and then into a 300 ml glass jar, allowing temperature equilibration. Outflows from the jars were connected to the Plexiglas blocks.
A digital video camera (Hitachi kP-D50, Tokyo, Japan, '' CCD,
768x494 pixels) with magnifying lens (Samsung 604CN, South Korea,
612 mm vari-focal zoom lens) was mounted above each Plexiglas block
inside the incubator and adjusted so that all 80 eggs were visible in the
frame of view. The experiment was carried out under constant illumination so
that eggs were continuously visible. Images from each camera were captured at
10-min intervals using a frame grabber (Model 3153, Data Translation,
Marlboro, MA, USA) controlled by image processing software (Global Lab Image/2
V3.0, Data Translation). Images were written to a hard drive, assembled into
movies, and analyzed for hatching time (±10 min). Hatching was obvious;
larvae emerged rapidly from their eggs and moved about their wells (see
supplemental material to view one of the movies).
Carbon dioxide emission
Carbon dioxide emission was measured using flow-through respirometry.
Batches of 40 3-day-old eggs (M. sexta) were weighed and placed into
a water-jacketed stainless-steel chamber sealed by a threaded steel screw
containing a built-in O-ring (custom built by the Department of
Chemistry's Machine Shop, University of Texas-Austin, USA). The steel chamber
was designed to interface with a gas multiplexer (TR-RM8, Sable Systems, Las
Vegas, NV, USA) in which the interior plastic tubing had been replaced by
brass and stainless steel. The multiplexer was also modified to accept steel
tubing from the jacketed chamber. The total internal volume of the air circuit
through the water jacket was 3 ml. Chamber temperature was controlled by
water from a recirculating bath (1160A, VWR, USA).
Gases were mixed from cylinders of O2 and N2 using calibrated mass flow controllers (Tylan FC-2900, Torrance, CA, USA and UNIT UFC-1100, Yorba Linda, CA, USA) and mixing electronics (MFC-4, Sable Systems). The stream (25 or 50 ml STPD min1) was directed past the eggs, through a small volume of indicating Drierite to remove water vapor, and into a carbon dioxide analyzer (CA-2A, Sable Systems). The analyzer was calibrated with pure N2 and 103.4 p.p.m. CO2 in N2 (Praxair, Danbury, CT, USA). Data were logged using Datacan V software (V5.4, Sable systems) receiving digital signals from an A/D converter (UI2, Sable Systems), which itself received analog signals from the instruments. In addition to CO2, we logged temperature in a separate chamber otherwise identical to the experimental chamber except that the steel screw supported a T-type thermocouple (connected to a TC-1000 thermocouple meter, Sable Systems) that extended into the chamber's air space.
We first measured CO2 emission from batches of eggs exposed to combinations of temperature and oxygen in a 4x7 factorial experiment (four temperatures: 22, 27, 32 and 37°C; seven oxygen levels: 5, 9, 13, 17, 21, 30 and 50 kPa). Individual batches of eggs were exposed to a single combination of oxygen and temperature (N=3 batches of 40 eggs at each combination) and then discarded. Eggs were equilibrated in flowing gas to each test temperature for 812 min, and the CO2 concentration (p.p.m.) was subsequently measured for 6.5 min. Mass-specific CO2 emission was calculated from concentration, flow rate and batch mass.
In a second experiment, we measured CO2 emission continuously while ramping the temperature from 16 to 48.5°C over 5560 min (0.57°C min1). By virtue of their small size, eggs have so little thermal inertia that they should always be in thermal equilibrium. The high temperature exceeded the upper thermal limit tolerated by eggs, but we wanted to stimulate maximal metabolic rates. Temperatures were ramped at four O2 levels, 11, 15, 21 and 30 kPa (N=3 batches of 40 3-day-old eggs at each level; 480 eggs total). For each ramp, average mass-specific emission rates were calculated at intervals of 1°C.
Internal oxygen partial pressure
Radial profiles of PO2 inside eggs were
obtained using a Clark-style O2 microelectrode with guard cathode
(model 737GC, 40 µm tip, Diamond General, Ann Arbor, MI, USA) connected to
a picoammeter (Chemical Microsensor I, Diamond General). The electrode was
calibrated in still water that was either air- or N2-saturated. The
water was held at constant temperature using a water-jacketed calibration cell
(custom made by the Department of Chemistry's Glass Shop, University of
Texas-Austin, USA) connected to a recirculating water bath. The electrode was
always calibrated at the temperature at which it would be used (24 or
37°C).
Eggs of M. sexta were affixed individually to double-sided tape so that the same surface that had been against the leaf was against the tape. In this orientation, the developing embryo was wrapped around the margins of the egg (parallel to the working surface). Under a dissecting microscope a fine insect pin was used to bore a small hole in the chorion. Subsequently, the electrode (calibrated before and after measurements from each egg) was placed through the hole using a micromanipulator (MM33, Märzhäuser, Wetzlar, Germany). The electrode was then advanced vertically down through the hole in 100 µm increments, for a total distance of 700 or 800 µm, about 300 µm past the egg's center. In this orientation, the electrode tip was advanced through the egg's center and avoided the embryonic tissue toward the lateral margins. Attempts were made to obtain readings in embryonic tissue, but these proved unreliable due to the difficulty of seeing tip placement through the chorion. Measurements were made on living eggs that were either <12 h or 3 days old (measured from oviposition, total development time at 27°C about 4 days) at either 24 or 37°C. As controls, 2- or 3-day-old eggs were killed by freezing (in liquid N2 or overnight in a 80°C freezer), thawed, then allowed to sit for 13 h at the test temperature (24°C only) before measurement of O2 profile.
Statistics
Statistics were done using S-Plus software (V6.1, Insightful Corp.,
Seattle, WA, USA). Egg survival was analyzed using logistic regression
(implemented in S-Plus using the generalized linear model function), which is
appropriate for data with a binary response variable (e.g. alive or dead)
(Armitage and Colton, 1998;
Selvin, 1998
). Survival data
were first fitted to a logistic regression model containing different
combinations of predictor variables, and the models were then tested for
significance by comparing how much additional deviance was explained by adding
a term (using a chi-square test). Egg development time was analyzed by linear
regression (using untransformed times) with temperature, oxygen, egg mass, and
their interactions as predictors. After initially fitting a full model
containing all possible interaction terms, a reduced model was constructed
that discarded all nonsignificant interaction terms from the first model.
Between 16 and 38°C, egg batches (three per temperature) from the
temperature ramping experiments emitted CO2 as an approximately
S-shaped function of temperature. For each batch of eggs, emission data were
therefore fitted (using the nonlinear least-squares function in S-Plus) by the
logistic curve:
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Results |
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Total development time (h) was affected by both temperature and oxygen (Fig. 1B). At 21 kPa O2, the Q10 of development rate (reciprocal of development time) was 2.3 between 22 and 27°C and 1.6 between 27 and 32°C (overall Q10 between 22 and 32°C was 1.9). We analyzed these data using linear regression, with temperature, oxygen and egg mass as predictors. In no preliminary analysis was egg mass significant, nor were any of the interaction terms including it. For all subsequent analyses (including those shown), egg mass itself was retained but all its interaction terms were excluded from the models. Two primary models were fitted. The first included development times of all eggs that hatched. Oxygen and temperature were highly significant (Table 3A), and the interaction between them, though explaining much less of the total variance, was also significant. The second model excluded eggs from the 9 kPa treatment, because only eggs from the lowest temperature treatment (22°C) withstood this degree of hypoxia. In the reduced dataset, both oxygen and temperature still were highly significant but their interaction was not (Table 3B).
|
Carbon dioxide emission
Linear regression revealed that temperature, O2, and their
interaction all significantly affected CO2 emission
(Fig. 2;
Table 4; fitted model: emission
rate = 2.89 0.64xoxygen level + 0.11 x temperature + 0.042
x oxygen x temperature, where oxygen level is in kPa and
temperature in °C). The significant interaction term reflects that at
higher temperatures, the effect of PO2 was more
pronounced (Fig. 2). Thus, at
37°C carbon dioxide emission rose more than fourfold between 5 and 50 kPa
O2, whereas at 22°C emission approximately doubled. In
addition, hyperoxia (30 and 50 kPa) led to higher emission rates only at
higher temperatures.
|
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During the temperature ramps, emission rates rose sigmoidally to a peak at about 38°C (Fig. 3). Rates subsequently dipped before rising to a second peak and then falling to zero. The same qualitative pattern appeared in all traces. Fig. 4 shows emission rates presented as functions of temperature (excluding rates beyond the trough, at 48°C). Clearly, higher O2 availability led to higher carbon dioxide production, most distinctly at the peak rates near 38°C. We analyzed this effect two ways. The simpler analysis consisted of two separate regression analyses of emission rates as a function of oxygen availability at either 16 or 38°C. PO2 had no effect at 16°C (F1,10=0.73, P=0.41), but did at 38°C [fitted model: emission rate = 15.9 + 0.61 x oxygen level (kPa); F1,10=22.5, P<0.001]. As a more complete analysis, we fitted emission traces from each batch of eggs with a logistic curve (Equation 1; model coefficients shown in Table 5). The coefficient with the most obvious biological meaning is K, which gives the asymptotic maximum emission rate. K was strongly and positively related to ambient oxygen availability (Fig. 5A). In addition, we used the fitted models to estimate emission rates at 16 and 38°C; those at 38°C were significantly related to PO2 where those at 16°C were not. To examine whether fitted models described the data adequately, we analyzed residual variation from each batch of eggs around its fitted model (Fig. 5B). Although the residuals had a tendency to exhibit a U shape (data above model predictions at low and high temperatures but below in between), most residual values were within 1 µmol CO2 g1 h1 of the model prediction, indicating a very good fit. Together, these analyses indicate that PO2 had an effect at high but not low temperatures.
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The location of peak emission rates was not affected by variation in PO2 (Fig. 4). However, the location of the post-peak trough in emission rate (right side of graph) occurred at a distinctly lower temperature at 11 kPa O2 than did the troughs at higher PO2 values.
Oxygen content
The electrode was stable and exhibited a stirring effect of only about 2%
(Fig. 6). Dead eggs showed
slight radial gradients of PO2
(Fig. 7). The cause of the
decline is unclear but may reflect interactions between the electrode tip and
yolk material or small rates of post-mortem O2 consumption
by persistent reactions. Living eggs showed much steeper
PO2 gradients than dead eggs
(Fig. 7; t-test of
live versus dead eggs at a distance of 500 µm, pooled across
stages and temperatures: t27=9.1,
P<0.001). PO2 values inside freshly
laid eggs (<12 h old) declined to 710 kPa at the center, where as
PO2 values inside 3-day-old eggs approached
zero. At both ages, eggs subjected to 37°C appeared to contain less oxygen
than those at 24°C. These effects were analyzed (positions 0500
µm for live eggs only) in a full ANOVA model, with position, age and
temperature as predictors, and taking into account the repeated measures
within eggs across positions (Table
6). The analysis confirmed the significance of the main effects of
age, position, and temperature. Two of the interactions (temperature x
age and position x temperature) were not significant, but two others
(position x age and the three-way interaction of position x
temperature x age) were highly significant. The biological
interpretation of these interactions is apparent from
Fig. 7. The interaction between
position and age reflects that PO2 values are
more divergent in center than in edge positions. The three-way interaction
reflects that in young eggs the main temperature-driven difference appears in
the central volume, whereas in old eggs it appears only in the first 200
µm.
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Discussion |
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Moreover, significant interactions between temperature and oxygen were apparent in most experiments. First, eggs experiencing relatively severe hypoxia were more likely to hatch when they developed at cooler temperatures (Fig. 1A). Second, metabolic rates were disproportionately affected by ambient oxygen availability at high temperatures, both at different steady-state combinations of temperature and oxygen (Fig. 2) and in experiments in which temperature was ramped gradually to very high values (Fig. 3). Third, both young and old eggs exhibited steeper radial oxygen profiles in warm (37°C) than in cool (24°C) temperatures. Together, these data strongly support the idea that oxygen limitation is more severe at high temperatures.
The sole instance in which an interaction did not emerge unequivocally was in the experiment on development time. Evaluating this dataset was complicated by the fact that development times could be measured only on surviving eggs and at the lowest oxygen level (9 kPa) only eggs from the coolest temperature (22°C) hatched. If these eggs were included in the regression analysis of development times, the temperatureoxygen interaction term was significant; if they were excluded, it was not. Over most of the range of experimental PO2 values, therefore, development times did not exhibit temperature-oxygen interactions. This result seems, at first glance, inconsistent with the metabolic and electrode data, which showed obvious interactions between the two variables. We suggest that the inconsistency stems from either of two interesting possibilities. First, the metabolic and electrode experiments exposed eggs to temperatures higher than the highest temperatures imposed in the developmental experiment (32°C); if oxygen is in increasingly short supply at high temperatures, we may simply have been more likely to see the interactions at temperatures above 32°C (though see Fig. 2). An alternative view is that temperatureoxygen interactions were stronger in the short-term experiments (metabolic and electrode experiments imposed experimental conditions for less than a few hours) than in the long-term experiments (the entire developmental period). This difference suggests that embryos receiving lengthy exposure to unusual combinations of temperature and oxygen may adjust their physiology or the gas transport characteristics of the eggshell layers.
Why, given their large surface area-to-volume ratios and short diffusion
distances, do eggs of M. sexta exhibit O2 limitation?
Barring some exceptions (e.g. Salt,
1952; Byrne et al.,
1990
), eggs of most terrestrial species do not have access to
water other than what is sequestered in the egg before oviposition. Water is
therefore a commodity not to be wasted. Retarding water loss, however, depends
on possessing a relatively impermeable eggshell, which in turn creates other
potential problems. In particular, no organism has evolved a barrier capable
of eliminating water loss while still conducting O2
(Hinton, 1953
), and therefore
water-resistant eggshells (essentially all terrestrial eggshells,
Hinton, 1981
) may pay the
price of reduced O2 delivery
(Smith, 1997
). Adults and
larvae or nymphs usually have access to water directly as free water or in
their food. Although pupae usually do not have access to water, they have much
lower surface area-to-volume ratios and may be protected from desiccation by
underground chambers, leaves, or cocoons.
Pörtner (2001,
2002
) argued that
O2 limitation at high temperatures results from the failure of
ventilation and circulation to deliver adequate oxygen to tissues. In
contrast, our electrode data strongly suggest that hot eggs of M.
sexta are limited by inadequate diffusive supply of
O2. In particular, the largest drop in
PO2 was observed just below the eggshell, and
most of the remaining drop occurred within 200 µm of the chorion
(Fig. 7). This result indicates
that the eggshell layers provided the largest resistance, but that the yolky
material surrounding the embryo was also a barrier to O2 flux.
Although later stage (day 4) embryos occasionally move, possibly causing
convective movement of egg liquids, we saw no indication of movement in the
stages used in our electrode experiments (< 12 h and 3-day-old).
Another question is what caused declining CO2 emission at
temperatures above 38°C. One possibility is that the declines stemmed
directly from low or falling internal PO2
(Pörtner 2001,
2001
). If so, however, the
temperature at which eggs exhibited maximal metabolic rates should have been
positively correlated with ambient PO2. In
fact, peak locations were similar across treatments, occurring at about
38°C at all four O2 levels
(Fig. 4). Declining
CO2 emission at temperatures >38°C instead must represent
direct effects of temperature on protein stability, or limitation by some
other unmeasured variable. It is conceivable that O2 affects
short-term tolerance to extreme high temperatures, but this possibility awaits
future tests.
Implications
The eggshell layers and arrangement of yolk and embryo are not particularly
unusual in M. sexta compared to other terrestrial insects
(Hinton, 1981), implying that
O2 limitation may be widespread among terrestrial insect eggs. Such
limitation could have interesting ecological and evolutionary consequences.
First, because water-resistant eggshells probably also restrict O2
flux (Hinton, 1953
),
evolutionary adjustment in eggshell structure among populations and species
may be closely related to trade-offs between retarding water loss and
obtaining sufficient O2
(Schmidt-Nielsen, 1984
).
Second, temperature-induced hypoxia may force warm-climate females to oviposit
only in relatively cool microclimates. This suggestion is particularly
relevant to desert populations of M. sexta. During their active
season in the Sonoran and Mojave deserts, daytime ambient air temperatures
often exceed 40°C. Smith
(1978
), however, showed that
leaves of some large-leafed desert perennials, including a host of M.
sexta, Datura metaloides, are cooler than ambient air,
apparently from high rates of transpiration. For example, on a day when the
air temperature was 43.7°C, leaf temperatures of D. metaloides
ranged from 26.136.3°C (matching well our range of experimentally
imposed temperatures). This finding suggests that the ecological success of
M. sexta in deserts even though M. sexta and most
other species of Manduca are primarily Neotropical
(Rothschild and Jordan, 1903
)
stems in part from the use of cool, large-leafed perennial host
plants.
Our data also suggest a novel hypothesis about Paleozoic insect gigantism:
hyperoxia during the late Carboniferous together with lower surface
temperatures (Berner, 1994;
Berner et al., 2003
) may have
facilitated the evolution of large eggs. Theoretical models and various
indirect data indicate that atmospheric oxygen content reached up to 35%
during the late Carboniferous (Berner et
al., 2003
). By increasing gradients driving diffusive
O2 flux, high ambient PO2 may have
facilitated the evolution of gigantism in numerous Paleozoic arthropods
(Graham et al., 1995
;
Dudley, 1998
), including
Paleoptera, Arachnida, the extinct Arthropleurida, and others (Shear and
Kukalová-Peck, 1989). Neontological tests of this hypothesis have
involved manipulation of oxygen availability and measurement of adult flight
performance and metabolic rates, but the results have been conflicting
(summarized by Harrison and Lighton,
1998
).
Selection on adult size, however, may not have been the only factor leading
to insect gigantism. In general, egg and adult size are positively correlated
within arthropod families (Fox and Czesak,
2000). For example, García-Barros
(2000
) used data from several
butterfly families to show that egg size (diameter) scaled to adult size (wing
length) by the relationship: egg size
adult size0.622. This
relationship indicates that small changes in egg size are associated with
large changes in adult size. Whether selection for larger egg size results in
correlated shifts to larger adult size, or vice versa, is unclear
(indeed the result could stem from selection on other correlated stages or
traits). Regardless, large eggs must be able to support embryonic development
with adequate oxygen flux clearly more easily done in hyperoxic
Paleozoic atmospheres. Future tests of this hypothesis should examine whether
eggs of other extant insect taxonomic groups are oxygen limited and whether
larger eggs (interspecifically) are more likely to show oxygen limitation. One
neontological example of the latter is provided by Belostomatidae
(Smith, 1997
), many of which
lay eggs that are very large. To obtain sufficient oxygen to support
development, these eggs must be actively ventilated by a parent or deposited
in air on emergent vegetation.
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Acknowledgments |
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Footnotes |
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Present address: Department of Integrative Biology, University of
California, Berkeley, CA 94720-3140, USA
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References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Alabaster, J. S. and Welcomme, R. L. (1962). Effect of concentration of dissolved oxygen on survival of trout and roach in lethal temperatures. Nature 194, 107.
Armitage, P. and Colton, T. (ed.) (1998). Encyclopedia of Biostatistics. Volume3 . Chichester: John Wiley & Sons.
Atkinson, D. and Sibly, R. M. (1997). Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol. Evol. 12,235 -239.[CrossRef]
Belehrádek, J. (1935). Temperature and Living Matter. Berlin: Borntraeger.
Berner, R. A. (1994). GEOCARB II: a revised model of atmospheric CO2 over Phanerozoic time. Am. J. Sci. 294,56 -91.
Berner, R. A., Beerling, D. J., Dudley, R., Robinson, J. M. and Wildman, R. A., Jr. (2003). Phanerozoic atmospheric oxygen. Ann. Rev. Earth Planet. Sci. 31,105 -134.[CrossRef]
von Bertalanffy, L. (1960). Principles and theory of growth. In Fundamental Aspects of Normal and Malignant Growth (ed. W. W. Nowinski), pp 137-259. Amsterdam: Elsevier.
Bradford, D. F. (1990). Incubation time and rate of embryonic development in amphibians: the influence of ovum size, temperature, and reproductive mode. Physiol. Zool. 63,1157 -1180.
von Buddenbrock, W. and von Rohr, G. (1923). Die Atmung von Dixippus morosus. Z. allg. Physiol. 20,111 -160.
Byrne, D. N., Cohen, A. C. and Draeger, E. A. (1990). Water uptake from plant tissue by the egg pedicel of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Homoptera, Aleyrodidae). Can. J. Zool. 68,1193 -1195.
Czerkies, P., Brzuzan, P., Kordalski, K. and Luczynski, M. (2001). Critical partial pressures of oxygen causing precocious hatching in Coregonus lavaretus and C. albula embryos. Aquaculture 196,151 -158.[CrossRef]
Daniel, S. H. and Smith, R. H. (1994). Functional anatomy of the egg pore in Callosobruchus maculatus: a trade-off between gas-exchange and protective functions? Physiol. Entomol. 19,30 -38.
Dudley, R. (1998). Atmospheric oxygen, giant
Paleozoic insects and the evolution of aerial locomotor performance.
J. Exp. Biol. 201,1043
-1050.
Ferguson, D. C., Harp, C. E., Opler, P. A., Peigler, R. S., Pogue, M., Powell, J. A. and M. Smith. (1999). Moths of North America. Jamestown, ND: Northern Prairie Wildlife Research Center Home Page. http://www.npwrc.usgs.gov/resource/distr/lepid/moths/mothsusa.htm. (Version 30DEC2002).
Fox, C. W. and Czesak, M. E. (2000). Evolutionary ecology of progeny size in arthropods. Ann. Rev. Physiol. 45,341 -369.[CrossRef]
Frazier, M. R., Woods, H. A., Harrison, J. F. (2001). Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiol. Biochem. Zool. 74,641 -650.[CrossRef][Medline]
Frederich, M. and Pörtner, H. O. (2000). Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am. J. Physiol. 279,R1531 -R1538.
García-Barros, E. (2000). Body size, egg size, and their interspecific relationships with ecological and life history traits in butterflies (Lepidoptera: Papilionoidea, Hersperioidea). Biol. J. Linn. Soc. 70,251 -284.[CrossRef]
Gehrke, P. C. (1988). Response surface analysis of teleost cardio-respiratory responses to temperature and dissolved oxygen. Comp. Biochem. Physiol. 89A,587 -592.[CrossRef]
Graham, J. B., Dudley, R., Aguilar, N. M. and Gans, C. (1995). Implications of the late Paleozoic oxygen pulse for physiology and evolution. Nature 375,117 -120.[CrossRef]
Greenlee, K. J. and Harrison, J. F. (2004).
Development of respiratory function in the American locust, Schistocera
americana. I. Across-instar effects. J. Exp.
Biol. 207,497
-508.
Hamor, T. and Garside, E. T. (1976). Developmental rates of embryos of Atlantic salmon, Salmo salar L., in response to various levels of temperature, dissolved oxygen, and water exchange. Can. J. Zool. 54,1912 -1917.[Medline]
Harrison, J. F. and Lighton, J. R. B. (1998).
Oxygen-sensitive flight metabolism in the dragonfly Erythemis
simplicicollis. J. Exp. Biol.
201,1739
-1744.
Hinton, H. E. (1953). Some adaptations of insects to environments that are alternately dry and flooded, with some notes on the habits of the Stratiomyidae. Trans. Soc. Br. Ent. 11,209 -227.
Hinton, H. E. (1981). Biology of Insect Eggs, Vol 1. Oxford: Pergamon Press.
Hoback, W. W. and Stanley, D. W. (2001). Insects in hypoxia. J. Insect Physiol. 47,533 -542.[CrossRef][Medline]
Keister, M. and Buck, J. (1961). Respiration of Phormia regina in relation to temperature and oxygen. J. Insect Physiol. 7,51 -72.[CrossRef]
Margaritis, L. H. (1985). Structure and Physiology of the Eggshell, Vol 1. Pergamon, Oxford.
Mills, N. E., Barnhart, M. C. and Semlitsch, R. D.
(2001). Effects of hypoxia on egg capsule conductance in
Ambystoma (Class Amphibia, Order Caudata). J. Exp.
Biol. 204,3747
-3753.
Orfanidou, C. C., Hamodrakas, S. J., Margaritis, L. H., Galanopoulos, V. K., Dedieu, J. C. and Gulik-Krzywicki, T. (1992). Fine structure of the chorion of Manduca sexta and Sesamia nonagrioides as revealed by scanning electron microscopy and freeze-fracturing. Tissue Cell 2, 735-744.[CrossRef]
Petersen, A. M., Gleeson, T. T. and Scholnick, D. A. (2003). The effect of oxygen and adenosine on lizard thermoregulation. Physiol. Biochem. Zool. 76,339 -347.[CrossRef][Medline]
Pörtner, H. O. (2001). Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88,137 -146.[CrossRef][Medline]
Pörtner, H. O. (2002). Climate variation and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp. Biochem. Physiol. 132A,739 -761.
Rothschild, L. W. R. and Jordan, K. (1903). A revision of the lepidopterous family Sphingidae. Novitates Zoologicae 9 Suppl.??? -???.
Salt, R. W. (1952). Some aspects of moisture absorption and loss in eggs of Melanoplus bivittatus (Say). Can. J. Zool. 30,5 -82.
Schmidt-Nielsen, K. (1984). Scaling: Why is Animal Size So Important? Cambridge: Cambridge University Press.
Selvin, S. (1998). Modern Applied Biostatistical Methods Using S-Plus. Oxford: Oxford University Press.
Seymour, R. S. and Bradford, D. F. (1987). Gas exchange through the jelly capsule of the terrestrial eggs of the frog, Pseudophryne bibroni. J. Comp. Physiol. 157B,477 -481.
Seymour, R. S., Geiser, F. and Bradford, D. F. (1991). Gas conductance of the jelly capsule of terrestrial frog eggs correlates with embryonic stage, not metabolic demand or ambient PO2. Physiol. Zool. 64,673 -687.
Shear, W. A. and Kukalová-Peck, J. (1990). The ecology of Paleozoic terrestrial arthropods: the fossil evidence. Can. J. Zool. 68,1807 -1834.
Sidell, B. D. and Hazel, J. R. (1987). Temperature affects the diffusion of small molecules through cytosol of fish muscle. J. Exp. Biol. 129,191 -203.[Abstract]
Smith, R. L. (1997). Evolution of paternal care in giant water bugs (Heteroptera: Belostomatidae). In The Evolution of Social Behavior Insects and Arachnids (ed. J. C. Choe and B. J. Crespi), pp. 116-149. Cambridge: Cambridge University Press.
Smith, W. K. (1978). Temperatures of desert plants: another perspective on the adaptability of leaf size. Science 201,614 -616.
Snyder, C. D. (1908). A comparative study of
the temperature coefficients of the velocities of various physiological
actions. Am. J. Physiol.
22,309
-334.
Snyder, C. D. (1911). On the meaning of
variation in the magnitude of temperature coefficients of physiological
processes. Am. J. Physiol.
28,167
-175.
Steiner, A. A. and Branco, L. G. S. (2002). Hypoxia-induced anapyrexia: implications and putative mediators. Ann. Rev. Physiol. 64,26 -288.
Tuft, P. H. (1950). The structure of the insect egg-shell in relation to the respiration of the embryo. J. Exp. Biol. 26,22 -34.
Wegener, G. (1993). Hypoxia and posthypoxic recovery in insects: physiological and metabolic aspects. In Surviving Hypoxia: Mechanisms of Control and Adaptation (ed. P. W. Hochachka, P. L. Lutz, T. Sick, M. Rosentahl and G.. van den Thillart), pp. 417-434. Boca Raton, FL: CRC Press.
Wood, S. C. (1991). Interactions between hypoxia and hypothermia. Ann. Rev. Physiol. 53, 71-85.[CrossRef][Medline]
Woods, H. A. (1999). Egg-mass size and cell size: effects of temperature on oxygen distribution. Am. Zool. 39,244 -252.
Zeh, D. W., Zeh, J. A., Smith, R. L. (1989). Ovipositors, amnions and eggshell architecture in the diversification of terrestrial arthropods. Quart. Rev. Biol. 64,147 -168.[CrossRef]
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