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Interactive Effects of Increasing Temperature and Decreasing Oxygen on Coastal Copepods

Abstract

The copepods of coastal seas are experiencing warming water temperatures, which increase their oxygen demand. In addition, many coastal seas are also losing oxygen because of deoxygenation due to cultural eutrophication. Warming coastal seas have changed copepod species’ composition and biogeographic boundaries and, in many cases, resulted in copepod communities that have shifted in size distribution to smaller species. While increases in ambient water temperatures can explain some of these changes, deoxygenation has also been shown to result in reduced copepod growth rates, reduced size at adulthood, and altered species composition. In this review we focus on the interactive effects of temperature and dissolved oxygen on pelagic copepods, which dominate coastal zooplankton communities. The uniformity in ellipsoidal shape, the lack of external oxygen uptake organs, and the pathway of oxygen uptake through the copepod’s integument make calanoid copepods ideal candidates for testing the use of an allometric approach to predict copepod size with increasing water temperatures and decreasing oxygen in coastal seas. Considering oxygen and temperature as a combined and interactive driver in coastal ecosystems will provide a unifying approach for future predictions of coastal copepod communities and their impact on fisheries and biogeochemical cycles. Given the prospect of increased oxygen limitation of copepods in warming seas, increased knowledge of the physiological ecology of present-day copepods in coastal deoxygenated zones can provide insights into the copepod communities that will inhabit a future warmer ocean.

Introduction

Coastal seas have experienced significant temperature increases over the past 50 years due to global warming (e.g., Najjar et al., 2010; Lehmann et al., 2011; Rice et al., 2015). Climate models suggest that these coastal seas will continue to warm significantly in the next 100 years (IPCC et al., 2019). The increasing water temperatures can result in a variety of stresses for aquatic fauna. At 20 °C there is ∼37 times less oxygen and 3 × 105 times lower diffusion rates in 30 psu seawater (at saturation) compared to air (e.g., Dejours, 1981; Verberk et al., 2011). It has been suggested that marine water breathers have evolved to live at their ambient dissolved oxygen conditions (Seibel and Deutsch, 2020). However, since the metabolism of marine ectotherms increases with temperature, warming seas will increase their oxygen demand while at the same time environmental oxygen availability is altered, with reductions in oxygen solubility lowering availability and increases in oxygen diffusivity and decreases in water viscosity increasing availability (e.g., Pörtner, 2010; Verberk et al., 2011). As temperatures increase, the linear increase in oxygen availability may initially satisfy the increase in oxygen demand of ectotherms; but because respiration is an exponential function of temperature, the oxygen demand may eventually outpace the rate at which it can be supplied, and the animals become oxygen stressed (Verberk et al., 2011, 2021). Faced with the multiple stresses of warming seas and potential oxygen limitation, marine ectotherms can adapt, move, or risk extinction.

In addition to the warming of coastal waters, cultural eutrophication causes hypoxia (i.e., a situation where oxygen saturation is below 100% air saturation) as a result of microbial respiration driven by enhanced organic loading (Diaz and Rosenberg, 2008; Breitburg et al., 2018). This deoxygenation of predominantly bottom waters has been shown to have a number of negative impacts on marine biota (Vaquer-Sunyer and Duarte, 2008; Ekau et al., 2010; Roman et al., 2019). Recent observations and models have shown that warming seas due to climate change are exacerbating these low-oxygen coastal waters by increasing the temporal and spatial extent and the severity of hypoxia (Conley et al., 2009; Altieri and Gedan, 2014).

The topic of this review is the interactive effects of increasing temperatures and decreasing dissolved oxygen on coastal marine copepods. As major consumers of phytoplankton and an essential food of higher trophic levels, copepods have a critical role in marine pelagic food webs (Steele, 1974; Verity and Smetacek, 1996). Copepods are considered one of the most abundant metazoan taxonomic groups on earth (Hardy, 1970; Turner, 2004) and include the orders Calanoida, Cyclopoida, and Harpacticoida. Most of our examples are from the Calanoida, which dominate coastal pelagic copepod communities and have a rich history of laboratory and shipboard experimental data on the effects of temperature and oxygen (reviewed in Mauchline, 1998; Roman et al., 2019). Copepods do not have specialized external organs for oxygen uptake, as do some other crustaceans. Their oxygen uptake occurs through pits in their body surface and in the hindgut (Marshall and Orr, 1955; Mauchline, 1998). We postulate that the size (mass, surface area, surface-to-volume ratio) of copepods likely reflects the ambient temperature along with oxygen supply and demand, with larger copepods more prone to oxygen limitation in warming coastal seas and seasonal hypoxic waters.

Temperature Effects on Copepods

Copepod body size in nature is inversely related to temperature, and this pattern is observed both within populations of the same species across their biogeographic range and across species from different latitudes (e.g., Deevey, 1960; McLaren, 1963; Uye et al., 1982). In controlled laboratory growth experiments with food usually in excess, marine copepods grown in warmer water are smaller in both length and weight as compared to the same species at the same stage reared at lower temperatures (e.g., McLaren and Corkett, 1981; Forster et al., 2011; Garzke et al., 2014; Doan et al., 2019). The size distribution of copepod communities is shifted to larger-sized species at higher latitudes (Mauchline, 1998; Brun et al., 2016; Evans et al., 2019; Campbell et al., 2021). In temperate seas the seasonal cohorts of copepods that occur in cooler temperatures are larger than the same species cohorts occurring when waters are warmer (Deevey, 1960; Heinle, 1966; Durbin and Durbin, 1978; Kimmerer and McKinnon, 1987; Lloyd et al., 2013; Horne et al., 2016; Pierson et al., 2016). Long-term time series in Long Island Sound have shown a significant decrease in the size of resident copepod species with warming waters associated with climate change (Rice et al., 2015). In the same geographic areas, changes in water masses due to large-scale climate patterns (i.e., North Atlantic Oscillation [NAO], El Niño-Southern Oscillation [ENSO]) have similarly resulted in shifts in the copepod community to smaller species in warmer water masses (Beaugrand et al., 2009; Lilly and Ohman, 2018). Thus, the inverse relationship between temperature and size is manifest at both individual species and community scales for copepods.

This ectotherm size distribution pattern as determined by temperature has been a foundation of ecology and was early observed by Bergmann (1847), who noted that warm regions tend to be inhabited by small-size species (Bergmann’s rule). The related James’s rule states that across populations of a species, populations found in warmer environments generally are smaller in body size (James, 1970). Atkinson (1994) postulated the temperature-size rule (TSR), which states that individuals of the same population grow to a smaller body size when reared at warmer temperatures. With both terrestrial and aquatic ecosystems already exhibiting warmer temperatures and grave concerns of how future warming will impact the earth, there have been renewed efforts to assess and model why the majority of ectotherms grow to a smaller size at warmer temperatures. However, there is still considerable debate about the controlling environmental factors and physiological mechanisms that support the TSR (e.g., Hoefnagel and Verberk, 2015; Lefevre, 2016; Pörtner et al., 2017; Ern, 2019; Rubalcaba et al., 2020; Einum et al., 2021; Deutsch et al., 2022). Here we confine our review to field and laboratory observations of copepods under different temperature and oxygen conditions to assess the potential impacts of warming seas on coastal copepods.

One early theory on why copepods are smaller at warmer temperatures was put forward by Miller et al. (1977), who synthesized growth studies of the marine copepod genus Acartia, which is common in coastal waters worldwide (Gonzalez, 1974). Using data from a variety of controlled laboratory growth experiments, Miller et al. (1977) speculated that the temperature-size response (Fig. 1A) is the result of temperature differentially affecting growth (i.e., increase in mass) and rate of molting (i.e., time available for growth). At higher temperatures, copepods proceed through molts faster, which outweighs the increase in growth rate. In contrast, the occurrence of larger copepods at lower temperatures is a consequence of much slower molting rates, such that the copepods can gain more mass between molts despite somewhat slower growth rates. More recently, Forster et al. (2011; Fig. 1B) explored different temperature-dependent growth and development models for copepods and also found that copepod development has a stronger temperature dependence (steeper slope) than does growth across all life stages, although their study revealed that response curves of growth and development with temperature were different in shape than found by Miller et al. (1977). The strongest differences in the temperature response of crustacean development and growth rates may be most evident in the late ontogenetic stages (Forster and Hirst, 2012). Horne et al. (2016) also investigated copepod growth and development, conducting laboratory growth experiments with four copepod species at three experimental temperatures. While temperature-dependent growth rates for the copepods varied with ontogeny, temperature-dependent development rates remained fairly constant between copepod development stages (Horne et al., 2016). The adult stages of all copepods studied were thus smaller at the higher temperatures presumably because molt rates increased faster than growth rates.

Figure 1. 
Figure 1. 

Relationships between copepod growth rate and molting rate as a function of temperature. (A) shows a conceptual model, modified from figure 8 in Miller et al. (1977), reprinted with permission from Wiley, and (B) shows statistical models estimated after an analysis of literature data, modified from Forster et al. (2011), using equations shown in their figure 3, after decentering their regressions.

The physiological basis of this difference for growth and development in ectotherms was suggested by van der Have and de Jong (1996), who pointed out that diffusion is less temperature sensitive than are enzymatic processes. Thus, because diffusion is the limiting rate for growth (protein synthesis), but enzymatic processes are the limiting rate for development (DNA replication), the growth rate of ectotherms is less sensitive to temperature than is their development. Note, however, that there is substantial complexity in both of these processes, involving complicated sequences of cellular and genetic control; and despite the generality of these mechanisms, the extent to which copepods exhibit size reductions in warmer water may differ across species. For example, in the study by Horne et al. (2016), adults of the largest copepod studied, the current-feeding calanoid Temora longicornis, exhibited the greatest temperature-size response (−4.16% °C−1), whereas the smallest temperature-size response was observed in the adults of the cyclopoid Oithona nana (−1.82% °C−1). The cyclopoid O. nana is an ambush-feeder, with reduced energy devoted to feeding compared to filter feeders and, subsequently, a lower oxygen demand (Lampitt and Gamble, 1982). This smaller species also has a higher surface-to-volume ratio than the larger copepod, which likely favors more efficient oxygen transport within the copepod. Another possibility is that there is a difference between Calanoida and Cyclopoida in their cell and genome size that may affect their oxygen limitation and potential temperature-size response (Verberk et al., 2021). Variation across copepod species in their temperature-size responses and their relationship with activity, body size, and cell size suggest that different oxygen requirements of growth and development that are temperature mediated (increased respiratory demand in relation to availability) could also result in smaller copepods.

The potential role of oxygen limitation of copepod growth and its effect on size is perhaps most apparent at warmer water temperatures found in the tropics, where the metabolic demand of copepods is high in relation to oxygen availability. The copepod Pseudodiaptomus annandalei in Southeast Asia is found in coastal waters that average 30 °C and experience 34 °C water during summer periods (Doan et al., 2019). The investigators grew the copepod at these water temperatures for three generations and found that the warmer water resulted in smaller adults (male and female) and reduced egg production (which in copepods is similar on a weight-specific basis to somatic growth) (Doan et al., 2019). Oxygen limitation of growth due to higher metabolic demand and decreased oxygen availability at warmer temperatures has been proposed as a mechanism to decrease ectotherm size with warmer seas (e.g., Verberk et al., 2011, 2021; Audzijonyte et al., 2019; Rubalcaba et al., 2020). The potential for oxygen limitation of growth is likely most apparent for hypoxic waters and for tropical copepods that are already living at a narrow margin of available oxygen meeting their metabolic demand.

Copepod Respiration

The respiration of copepods is typically an exponential function of temperature, at least up to some upper temperature (Ikeda, 1970). While there are differences between species, thermal ranges, and acclimation periods, published values of Q10 for copepod respiration range from 1.0 to 2.7 (Mauchline, 1998; Teuber et al., 2013). Temperature also influences the oxygen availability to copepods. While oxygen solubility in seawater decreases with increasing temperature (Dejours, 1981), maximum rates of oxygen diffusion increase in a linear fashion with increasing temperature (Verberk et al., 2011). In addition, warmer water is less viscous, which thins the boundary layer that can limit diffusion across the surface integument for copepods (Verberk et al., 2021). These increases in diffusion and transport may initially satisfy the increased oxygen demand by copepods; but because respiration is an exponential function of temperature, the oxygen demand eventually exceeds the availability, and animals may become oxygen stressed (Verberk et al., 2011). Thus, warming seas have the potential to tip the balance of oxygen demand exceeding oxygen supply for copepods, as has been postulated for other ectotherms (e.g., Daufresne et al., 2009; Audzijonte et al., 2019; Rubalcaba et al., 2020).

The metabolic activity and respiration of copepods scale allometrically with body size, with an exponent <1. As a result, when expressed per mass unit, respiration decreases with body size (see reviews by Marshall, 1973; Hirst and Sheader, 1997; Mauchline, 1998). Thus, for comparing the respiration of different developmental stages of a particular species as well as comparisons of different copepod species across wide size ranges, investigators have developed empirical allometric models that predict respiration rates from body mass (e.g., Raymont and Gauld, 1951; Marshall, 1973; Ikeda, 1985). Since oxygen uptake by copepods takes place through the integument, smaller copepods with a higher surface-to-volume ratio may be favored in warmer waters, where respiratory demand is higher. Similarly, in low-oxygen environments, smaller copepods may be favored because of their potentially more efficient oxygen diffusion to their internal circulatory system (Roman et al., 2019). Although mass-specific metabolic rates are higher in small copepods (as highlighted above), the increase in oxygen demand with size (mass-scaling exponent ∼0.8) exceeds the increase in surface area (mass-scaling exponent ∼0.7), such that the balance between oxygen demand and supply may deteriorate for larger copepods (Einum et al., 2021). Note that the mass-scaling exponent for oxygen supply may be even lower when accounting for boundary layer effects (Deutsch et al., 2022). Ikeda (1974) compared the respiration rates of copepods from boreal, temperate, subtropical, and tropical waters (average water temperatures 8.6, 15.0, 20.2, and 26.8 °C, respectively) and found that slope of the regression of oxygen consumption against copepod body weight increased with temperature, proceeding from boreal to subtropical waters, but decreased at the warmest temperatures for copepods in tropical waters (Ikeda, 1974). Thus, in the warm tropical waters, rates of oxygen uptake decreased for the larger copepods relative to the smaller copepods. The higher metabolic demands in the tropical waters relative to oxygen supply may have been most acute for the larger copepods, with a lower surface-to-volume ratio, larger cell size, and less efficient oxygen uptake. Thus, respiration appears to become more oxygen limited for larger copepods.

Synthesis of data from multiple copepod species has shown that body mass and habitat temperature can account for 72%–96% of measured weight-specific copepod respiration rate (Ikeda, 1985; Ikeda et al., 2007; Bode et al., 2013). Thus, for copepods, most of the variation in metabolic rate relates to variation in size and temperature rather than species-specific differences (Huntley and Lopez, 1992; Hirst and Sheader, 1997). Note, however, that there are examples of particular species or copepod groups (i.e., cyclopoid copepods; Lampitt and Gamble, 1982) that have lower weight-specific respiration rates because of their slower swimming and feeding behavior. It is not surprising, given their lower oxygen demand, that cyclopoid copepods have been shown to be abundant in low-oxygen waters (Uye, 1994; Elliott et al., 2012; Roman et al., 2019) and tropical systems, and that they are becoming more abundant in coastal waters that have been warming due to climate change (Rice et al., 2015). Further research is warranted to elucidate the possible roles of cyclopoid behavior, as well as higher surface-to-volume ratio and smaller cell or genome size, which may favor them in warmer coastal seas.

Copepods in Low-Oxygen Waters

Given the likelihood of increased oxygen limitation of copepods in warming seas, it is instructive to review results from both field observations and laboratory experiments on low-oxygen impacts on copepod ecology and physiology to gain some insights into the copepod community structure in a future warmer ocean. While a variety of physiological adaptions to low-oxygen conditions have been described for open-ocean zooplankton with permanent low-oxygen zones, coastal zooplankton experience hypoxia that varies in severity on daily to seasonal time scales. Oxygen-binding proteins that have the potential to enhance survival at low-oxygen conditions have not been identified in copepods (Thuessen et al., 1998). Without gills or hemoglobin, options for adapting to low-oxygen conditions are more limited for coastal copepods.

Laboratory experiments

Low-oxygen water (<2 mg L−1) generally reduces the survival of copepods under controlled laboratory conditions (Vargo and Sastry, 1977; Roman et al.,1993, Stalder and Marcus, 1997; Marcus et al., 2004; Richmond et al., 2006) and has been demonstrated to severely reduce the hatching success of copepod eggs in several species (Lutz et al., 1992; Roman et al., 1993; Marcus et al., 1994, 1997; Marcus and Lutz, 1994; Invidia et al., 2004; Richmond et al., 2006). Under controlled laboratory conditions, Marcus et al. (2004) and Richmond et al. (2006) showed that egg production and population growth rate in the ubiquitous coastal and estuarine calanoid copepod Acartia tonsa were reduced in low-oxygen waters (0.7 and 1.5 mL O2 L−1) compared to normoxic controls. It is interesting to note that the sizes of both male and female adult copepods reared in the low-oxygen conditions were smaller than those in normoxic conditions (Richmond et al., 2006; Fig. 2). The smaller-sized copepods were the result of the oxygen-limited growth rates (Richmond et al., 2006). Thus, we see that deoxygenation can also reduce copepod size, most likely because of lower growth rates.

Figure 2. 
Figure 2. 

Size (volume) of Acartia tonsa stages grown at three different oxygen levels and two temperatures. The figure was modified from figure 5 in Richmond et al. (2006), reprinted with permission from Elsevier, and includes their panels (B) and (D), showing their experiments 2 and 4. (A) is from summer experiments at 25 °C, and (B) is from winter experiments at 15 °C. Symbols show mean (±SD) data, with dark gray lines and X symbols from the lowest oxygen concentration (0.7 mL L−1), light gray lines and filled circles from the middle oxygen concentration (1.5 mL L−1), and black lines and triangles from the saturating oxygen concentration. Oxygen concentrations were converted to partial pressure at experimental temperature and salinity (30), using equations from Myers (2011) and references therein. Estimates of critical oxygen partial pressure (Pcrit) and lethal oxygen partial pressure (Pleth) are from Elliott et al. (2013). Life stage includes nauplii, copepodite I, II, III, IV–V, and adult males and females.

Using both data from the literature and laboratory measurements, Elliott et al. (2013) showed that reduced oxygen limited a variety of vital rates of the copepod A. tonsa. Egg production, somatic growth rates, and ingestion were all reduced with lower oxygen partial pressures (Fig. 3). Below an oxygen pressure of 8.1 kPa (Pcrit, critical oxygen partial pressure) at 18 °C, respiration rates decrease linearly until the lethal oxygen partial pressure (Pleth), 3.7 kPa (Elliott et al., 2013). Acartia tonsa has been reported to occur at temperatures from −1 °C to 32 °C (Gonzalez, 1974). Assuming a Q10 of 2.03 for A. tonsa oxygen demand (Gaudy et al., 2000), this temperature range corresponds to a range of estimated Pcrit values from 2.5 to 20.8 kPa (∼1.5 to 6.2 mg L−1). Note that Pcrit is also determined by oxygen supply, which is influenced by temperature, so that scaling it using only the Q10 to describe the increase in oxygen demand with temperature does not consider the increase in oxygen supply with temperature (Verberk et al., 2011).

Figure 3. 
Figure 3. 

Relationship between Acartia tonsa respiration rate and oxygen partial pressure, modified from Elliott et al. (2013). Symbols represent mean data from experimental determination of different vital rates collected at varying oxygen concentrations, and error bars show ±SD. Original data were converted to respiration rates by using the conversions provided in table 1 of Elliott et al. (2013), and oxygen concentrations were converted to partial pressures. Vital rates are abbreviated R (respiration), EP (egg production), G (growth), and I (ingestion), and references are abbreviated K1985 (Kiørboe et al., 1985), M2004 (Marcus et al., 2004), R2006 (Richmond et al., 2006), SM2005 (Sedlacek and Marcus, 2005), and E2013 (Elliott et al., 2013). Details and data are found in Elliott et al. (2013 and associated supplementary information).

Field observations

Copepods differ in their sensitivity to hypoxia. There have been a variety of copepod abundance patterns observed in coastal waters experiencing bottom-water hypoxia (see reviews by Roman and Pierson, 2019; Roman et al., 2019). While some low-oxygen bottom waters are avoided by copepods, in other hypoxic areas copepods reside in the low-oxygen bottom waters for various time periods. A key factor in understanding these different spatial patterns is the temperature of the low-oxygen waters. For example, in the Gulf of Mexico, copepods show strong avoidance of low-oxygen bottom waters (Roman et al., 2012), where water temperatures can exceed 28 °C (Pierson et al., 2009). In contrast, copepods reside in low-oxygen waters of the Baltic Sea for much of the day (Appeltans et al., 2003; Webster et al., 2015), where water temperatures are 8 °C to 10 °C (Carstensen et al., 2014). A concentration of 2 mg L−1 bottom water in the Baltic (9 °C) would have an oxygen partial pressure of 4.2 kPa, which is slightly below the limiting Pcrit of A. tonsa predicted by Elliott et al. (2013) for this temperature (5.07 kPa). In contrast, 2 mg L−1 bottom water in the Gulf of Mexico (30 °C) would have an oxygen partial pressure of 6.4 kPa, which is significantly below the limiting Pcrit of A. tonsa predicted for this temperature (18.3 kPa) and about the same as the predicted lethal oxygen concentration (Pleth = 6.8 kPa). These predicted differences in oxygen availability and demand as parametrized in Pcrit enable us to assess how dissolved oxygen and water temperature jointly determine habitat availability for coastal zooplankton in hypoxic water and warmer waters in future climate change scenarios (e.g., Deutsch et al., 2015).

Besides increasing the temporal and spatial extent of coastal hypoxic waters, warming seas will also increase the metabolic demand of copepods, thus making deoxygenated waters less hospitable. A meta-analysis for marine benthic organisms suggested that a 4 °C temperature increase for shallow coastal waters (which are warming more rapidly than the global ocean) would reduce survival times in hypoxic waters by 36% and increase the threshold of lethal oxygen concentrations by about 26% (Vaquer-Sunyer and Duarte, 2011). Using the same potential temperature increase of 4 °C by the end of the twenty-first century, coastal copepods would increase their respiration about 40% (assuming a Q10 of 2.3) or 31%, using the average value of 7% per degree Celsius by Heine et al. (2019). This higher respiratory demand will make deoxygenated bottom waters less of a refuge from predation for copepods and also increase the mortality of copepod eggs that sink into the low-oxygen bottom waters (Roman and Pierson, 2020).

The constraints on acquisition of oxygen by coastal copepods do not preclude some adaptations and genetic differences between taxa in response to deoxygenation. Recent work has highlighted how thermal tolerance in the calanoid copepod A. tonsa increased over many generations in a laboratory culture, at the cost of plasticity in thermal tolerance (Sasaki and Dam, 2019, 2021). Similar studies have not been done on deoxygenation effects. Additionally, the impact of cryptic species on our comparisons across taxa cannot be discounted. Two of the dominant coastal copepod genera, Acartia and Eurytemora, have well-documented cryptic speciation (Lee, 2000; Lee and Frost, 2002; Chen and Hare, 2008, 2011; Plough et al., 2018). In these cases, the genetic basis for determination of cryptic speciation is done with neutral markers that are not directly relevant to the response to deoxygenation or increasing temperature. There may be a scope for genetic adaption of hypoxia tolerance in coastal copepods that has yet to be examined.

Integration of Temperature and Oxygen Effects on Coastal Copepods

As detailed previously, temperature and oxygen interactively influence copepod growth rate and molting rate, which together determine adult size and egg production. Therefore, assessing copepod ecology in warmer coastal seas as result of climate change should try to incorporate both oxygen and temperature effects on copepod physiology and population dynamics. Recent data syntheses suggested that copepod respiration rate increases by about 7% per degree Celsius (slope = 0.0751) (Heine et al., 2019), whereas copepod growth rates increase by about 2% per degree Celsius (slope = 0.0208) (Hirst and Lampitt, 1998). If this difference is real, it suggests that in warming seas the respiration of copepods will increase faster than their growth rates. However, responses by particular species may be affected by the temperature range they experience and their thermal tolerance. Laboratory experiments with individual copepod species have shown that respiration as a function of temperature can have a sigmoidal response, with slopes decreasing or becoming negative at higher temperatures that are at the limit of or exceed the copepods’ temperature range (Alejandro et al., 2008; Castellani and Altunbas, 2014). Thus, the measured response of copepod respiration to warming may vary, depending on habitat temperature and thermal tolerance limits.

Several investigators have conducted laboratory experiments by using different temperature and dissolved oxygen concentrations to assess the impacts on the common coastal copepod Acartia tonsa (Marcus et al., 2004; Sedlacek and Marcus, 2005; Richmond et al., 2006). We synthesized these studies and converted rates of weight-specific copepod egg production to weight-specific growth rates (d−1), as has been shown to compare to the somatic growth of juvenile stages for A. tonsa (Berggreen et al., 1988). Copepod growth rates at the highest dissolved oxygen concentrations show the expected effects of higher growth rates with increasing temperature. However, at lower oxygen concentrations, the higher respiratory demands of copepods in the warmer waters (higher Pcrit) result in reduced growth rates, so that the effects of higher temperatures on growth are negated by greater respiratory demand. At the lowest temperature, copepod growth rates were less impacted by reduced oxygen content (lower slope; see Fig. 4).

Figure 4. 
Figure 4. 

Relationship between Acartia tonsa growth rate (d−1) and oxygen partial pressure (pO2 [kPa]) measured at three temperatures. Data are presented as symbols and regressions as lines for pO2 at 15 °C (blue triangles, small dashed lines), 20 °C (black squares, large dashed lines), and 25 °C (red circles, solid lines), with the values of critical oxygen partial pressure (Pcrit) at each temperature indicated as arrows. Slopes of all regressions were significantly different from zero (15 °C: P = 0.00034, R2 = 0.562; 20 °C: P = 0.00074, R2 = 0.597; 25 °C: P = 6.4 × 10−15, R2 = 0.889).

Copepod Size and Ambient Oxygen and Temperature

The uniformity in ellipsoidal shape (Fig. 5), the lack of external oxygen uptake organs, and the pathway of oxygen uptake through the copepod’s integument make calanoid copepods ideal candidates for an allometric approach to predict copepod size with increasing water temperatures and decreasing oxygen in coastal seas. There is a rich literature for phytoplankton suggesting that smaller cells have increased surface-to-volume ratios, making them more competitive at resource acquisition in low-nutrient environments (e.g., Chisholm, 1992; Kiørboe, 1993; Raven, 1998). Lower oxygen availability may favor copepods with better oxygen uptake capacity, which could relate to both cell size and body size. Smaller cell size in smaller copepods within a given species and stage may lead to an increased capacity, because oxygen needs to be transported across the cell membrane to the mitochondria; and for smaller cells there is greater surface area and shorter diffusion distances (Verberk et al., 2021). Smaller body size also translates into a greater surface area-to-volume ratio to favor more efficient oxygen transport. The surface-to-volume ratio of some representative copepods varies by over an order of magnitude (Table 1), with the larger Calanus copepods found in cooler waters, smaller Acartia found in warmer waters (both in the order Calanoida), and small ubiquitous Oithona (in the order Cyclopoida) found in nearly all marine systems and especially in tropical systems. In general, smaller copepods with a higher surface-to-volume ratio are found in warm tropical waters and in waters where oxygen has been reduced because of cultural eutrophication.

Figure 5. 
Figure 5. 

Size and shape of various calanoid copepods. Copepods are identified from the top and left to right as Acartia sp., Calanus finmarchicus, Rhincalanus nasutus, Pseudeuchaeta brevicauda, Aetideopsis multiserrata, Gaetanus latifrons, Cephalophanes refulgens, and Bathycalanus princeps. Modified from figure 2 in Mauchline (1998), with permission from Elsevier.

Table 1. 

Surface area (mm2), volume (mm3), and surface area-to-volume ratio for several copepod species, assuming copepod shape is an ellipsoid (Mauchline, 1998)

CopepodSurface area (mm2)Volume (mm3)Surface area-to-volume ratio
Calanus finmarchicus6.40141.15165.56
Centropages hamatus0.73000.047215.47
Acartia tonsa0.56240.030118.68
Oithona similis0.22840.007530.41
Microsetella norvegica0.08030.001359.93

There have been a number of global analyses on marine copepod metabolism, including growth, development, and respiration rates, which have shown that body size transcends species differences in metabolic rates (e.g., Ikeda, 1985; Huntley and Lopez, 1992; Hirst and Lampitt, 1998). Thus, investigators have used allometric models to predict environmental effects on copepod metabolism and their impact on community structure and function (e.g. Ward et al., 2012). If the ability to cope with higher metabolic demand and lower oxygen availability is favored in smaller copepods with a higher surface-to-volume ratio, this may be reflected in lower Pcrit values with size (Fig. 6). More research is needed to elucidate the Pcrit of various coastal copepod species and determine whether it scales with properties of body mass (volume, surface area, surface-to-volume ratio). Note, however, that the use of Pcrit to predict ectotherm physiology to lower oxygen availability has been criticized recently (Wood, 2018; Seibel and Deutsch, 2020). However, given that experiments that measure Pcrit for the relatively small coastal copepods (100 μm to 5 mm) are done with animals swimming in small containers and thus not at their resting metabolic rate, this may counter one major criticism of the use of Pcrit as a metric of deoxygenation effect. More information about the effects of oxygen and temperature on copepods is likely to be obtained with the inclusion of additional metrics, such as maximum respiration rate, aerobic scope, or other physiological condition indices. Additional measurements and analyses are needed to elucidate the mass scaling of copepod oxygen uptake capacity and compare it to the mass scaling of oxygen demand. Our prediction that copepods with a higher surface-to-volume ratio are favored in low-oxygen environments is reversed if respiration rate increases more slowly with body mass than does the surface-to-volume ratio, as has been found for salmonid eggs (Einum et al., 2002). For copepods, differences between stages and species should also be included in any such analyses.

Figure 6. 
Figure 6. 

Conceptual model of copepod weight-specific respiration rate as a function of oxygen partial pressure (pO2) for different-sized copepods. Thick solid lines show the hypothesized oxygen-dependent respiration rate for small (light purple) and large (dark purple) copepods. Shaded areas show the region where the respiration rate is not limited by environmental pO2. Solid horizontal lines show standard metabolic rate (SMR). X symbols show the pO2 at lethal oxygen partial pressure (Pleth) for both sizes of copepod. Vertical dotted lines show the pO2 at critical oxygen partial pressure (Pcrit; large dashes) and Pleth (small dashes) for each copepod size. Red arrows are used to show how both Pcrit and Pleth are hypothesized to increase with increasing size.

If we can establish how Pcrit or some other oxygen tolerance metric scales with copepod mass, we can then develop generalized, functional relationships that describe and quantify the interactive effects of temperature and low oxygen on coastal zooplankton. This information will lead to improved size-structured models to predict the effects of increasing temperatures and decreasing oxygen on pelagic food webs. Such models will be important to assess the climate-induced changes in the size distribution of the copepod community on fisheries (McGinty et al., 2021).

Conclusions

The environmental and physiological mechanisms that result in reductions in the size at maturity of copepods living in warmer water may be key in helping them adapt to the increased respiratory demand and reduced oxygen solubility. This smaller size, both for the entire individual and perhaps also for the size of the individual cells that make up the individual, will potentially increase oxygen transport capacity, lowering their Pcrit and thus reducing the oxygen limitation of growth and reproduction. Warming oceans may elicit a response from copepods ranging from reduced size, activity, growth, and cell size that allows them to adapt to the lower oxygen partial pressure, as has been suggested for aquatic ectotherms (Verberk et al., 2021). More research is needed to test whether oxygen tolerance estimates for growth, reproduction, and metabolism, using Pcrit or another metric, scale with copepod size (mass, volume, surface area, surface-to-volume ratio). If such relationships exist, copepod size-structured models can be constructed to predict future coastal copepod communities.

More research is needed to elucidate the physiology and ecology of tropical copepods that likely are already living at their thermal maximum at reduced oxygen solubilities. Cyclopoid and harpacticoid copepods often make a greater contribution to tropical and sub-tropical copepod communities, yet in general most of our knowledge of copepod physiological ecology comes from studies of calanoid copepods in temperate waters. As such, fruitful research directions include elucidating the behavioral and physiological adaptations that cyclopoid and harpacticoid copepods will have to deal with, such as heat and hypoxia, as well as how oxygen supply and demand scale with their reduced body mass.

Our research on various projects that focused on the effects low oxygen on copepods provided background for the manuscript. We gratefully acknowledge the following support: National Oceanic and Atmospheric Administration-Northern Gulf of Mexico Ecosystems and Hypoxia Assessment (NOAA-NGOMEX) NA06NOS4780148 and NA09NOS4780198 and National Science Foundation OCE-0961942 and OCE-1259691 and National Academy of Sciences NAS-2000006418. This manuscript was improved by the helpful suggestions of two anonymous reviewers.

Abbreviations

  • Pcritcritical oxygen partial pressure
  • Plethlethal oxygen partial pressure

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