Impact of thermal variation on the naupliar development of the copepod Apocyclops spartinus (Ruber, 1968) (Copepoda: Cyclopidae), under controlled conditions

ABSTRACT

Apocyclops spartinus is a subtropical resilient copepod from impacted Peruvian wetlands, widely used for marine fish larviculture and conserved as a strain at Instituto del Mar del Peru - IMARPE. This study was conducted to test the effects of three thermal conditions (16, 20 and 24 ºC) on the individual growth of conditioned nauplii. Sub-stage growth rates, three growth models and three growth rate-dependent models were evaluated. Considering these previous experiments, naupliar growth retardation and mortality were evaluated for cold shock stress (8 ºC lower). Results indicated a progressive increase in development time by reducing temperature from 24 to 20 ºC (1.75 times) and 20 to 16 ºC (4 times). Growth rates showed a tendency to decrease, prior to metamorphosis and independent of temperature. Gompertz was the best growth model by describing sigmoidal tendency of naupliar development. Arrhenius was the best growth rate-dependent model but slightly better supported than a simple allometric model. Naupliar growth retardation was noted in nauplii that were initially hatched at 24 ºC and then swiftly transferred to a culture at 16 ºC. This cold shock stress resulted in high mortality from day four onwards. In summary, A. spartinus nauplii exhibit potential as a live food source and it is recommended that targeted thermal treatments be employed to extend the time of optimal nauplii size and thereby enhance culture techniques of this species.

Keywords:
Copepod; cold stress; growth model; growth rate; naupliar measurements

INTRODUCTION

Planktonic copepods are small but fundamental organisms and stand out as hydrobiological resources of great value within food webs (Turner, 2004). Their role lies in being part of the natural diet of numerous marine species. This fact underlines the importance of developing culture techniques, which allow prediction of development, especially in the naupliar stage (Ajiboye et al., 2011). This stage is crucial since their small size makes them an ideal live food for the first larval feeding of fish and crustaceans, due to their incompletely developed digestive system (Naman et al., 2021).

Copepods represent an essential nutritional source for fish larvae, thanks to their protein and fatty acid content, as well as their richness in vitamins and antioxidants such as vitamin E, vitamin C, and astaxanthin; as reported in Acartia Dana, 1846, Centropages Krøyer, 1849, and Eurytemora Giesbrecht, 1881 (van der Meeren et al., 2008). Furthermore, their ability to adjust lipid accumulation in response to environmental conditions (Skottene et al., 2020), along with consistency in their behavioral and reproductive patterns under stable conditions (Drillet et al., 2011), makes them keystone organisms for aquatic ecosystems and aquaculture.

On the other hand, it is important to evaluate copepods under stressful conditions, looking for potentialities such as high lipid levels (Goolish and Burton, 1989). The adaptive effect of copepod population and gene expression upon changes in thermal stress has been clearly observed in cultures where gene flow is restricted (Schoville et al., 2012). The pace of organism lifespans is driven by the magnitude of a specific metabolic rate, which includes the timing of each event, such as hatching or growth (Brown et al., 2004). Therefore, descriptions of growth rates are considered metabolic consequences of many different biological reactions (Gillooly et al., 2001). Sasaki and Dam (2021) suggested that evolution of increases in thermal tolerance reduces the capacity for acclimation to new conditions, and they reported that intertidal and freshwater copepods generally have higher thermal tolerance than marine copepods.

Studies on copepod production are just beginning using species with aquaculture potential, such as the genus Apocyclops Lindberg, 1942 from inland saline habitats in Central Asia and Iran (Farhadian et al., 2009), or marine genera such as Acartia in the USA (Sarkisian et al., 2019), Euterpina acutifrons Dana, 1847 in Borneo (Amatus et al., 2020), Tigriopus Norman, 1869 in Ireland (Prado-Cabrero et al., 2022), and Oithona Baird, 1843 in India (Santhanam et al., 2019). Species of the genus Apocyclops are studied as live food. In Asia, Apocyclops dengizicus Lepeshkin, 1900 is cultured under optimal conditions of 35 °C and salinity 20 PSU (Farhadian, 2006; Farhadian et al., 2007) and Apocyclops royi Lindberg, 1940 under 28 °C and salinity 20 PSU (Pan et al., 2016). While in North America there is a record of experimental culture of Apocyclops panamensis Marsh, 1913 (Cruz-Rosado et al., 2020) under an optimum temperature of 32 °C, explaining its natural tropical occurrence. However, it can be adapted to temperatures lower than 20 °C. In Venezuela, Apocyclops distans Kiefer, 1956 were tested with three different diets in laboratory conditions (Velásquez et al., 2001). In Peru, studies are being carried out using two reference strains of microalgae and the local copepod A. spartinus (as Apocyclops sp.) (Alejos-Cabrera et al., 2022) which have served to improve feeding strategies for fish and marine crustaceans of importance in aquaculture (Carrera et al., 2018; Montes et al., 2019).

The copepod in this research paper was originally collected from wetland environments on the central coast of Peru, that are now facing serious environmental issues, such as seasonal eutrophication caused by the accumulation of sewage flows (Vizcardo and Gil-Kodaka, 2015). This eutrophication is characterised by the water being a green color and the distinctive smell of stagnant water (Romero-Mariscal et al., 2023). Research on such species found in fragile ecosystems can also encompass evaluating their hydrobiological resource potential to support habitat preservation efforts (Carranza-Castillo et al., 2021; Sánchez-Dávila et al., 2021).

This study aims to characterise and model the naupliar development of the copepod A. spartinus at three temperatures and to evaluate its growth response to cold stress under laboratory conditions. Through this research, we seek to contribute to a better understanding of the biology of this copepod and its possible applications in aquaculture and conservation.

MATERIAL AND METHODS

Copepod sampling

Adult copepods were collected from the Municipal wetland of the district of Ventanilla, Callao, Peru, in 2009. The sampling station was recorded using a Garmin GPS, model GPSMAP 60CSx (Shijr, New Taipei City, Taiwan), and the data used for mapping was WGS1984 (11°52′16.11″S 77°08′17.88″W). A surface trawl was towed with a 10 µm phytoplankton net and the collected organisms were transported in 250 ml plastic containers to the laboratory of the Germplasm Bank of Aquatic Organisms (BGOA, Spanish acronym) of Instituto del Mar del Peru (IMARPE).

Conditioning and culture of copepod stocks

Adult females and males were isolated to initiate the discontinuous monoculture with the preservation code IMP-BG-Z014. Copepods were isolated by successive pipetting and washing between drops of filtered and sterile seawater on a glass slide, based on Andersen (2005). The strain is conserved ex situ at the BGOA (http://www.imarpe.pe/imarpe/index2.php?id_seccion=I0170050400000000000000, accessed on October 17, 2023). The isolated male and female copepods were placed in a beaker with sterile water at 12 PSU and 20 °C. After 2 weeks, copepods were progressively conditioned until reaching 35 PSU and 24 °C, which are the conditions needed to feed marine fish larvae. The copepods were maintained inside a Torrey R-14AI climatic chamber under controlled conditions of temperature (24 ± 1 °C), illumination (60 µM s^-1m^-2), 14:10 h photoperiod (light:dark) and salinity of 35 PSU without aeration. Replacement seawater was filtered at 0.22 µm and heat sterilized gradually to reach 105 °C for 10 min. Copepods were cultured in 500 ml beakers at a density of 1 copepod/ml. Once a week, there was a 100% water renewal using the sterilized seawater. Yucra (2008) pointed out that diatoms were the dominant microalgae in the original habitat, although previous pilot feeding experiments showed A. spartinus preferred motile microalgae, such as Tetraselmis spp. For this reason, the experimental copepods were fed weekly with the microalgae Tetraselmis sp. (10⁴ cell/ml).

Microalgae culture

The strain used was Tetraselmis sp., which was cultivated at BGOA, at a volume of 200 ml in batch culture mode with Guillard F/2 (Guillard, 1975). Cultures were maintained under controlled conditions of ambient temperature (17 ± 1 °C), light intensity of 35 ± 5 μM m^-2 s^-1 with 12:12 h photoperiod (light: dark), pH 7 ± 1, salinity of 35 PSU and with constant agitation at 100 RPM through a PRO VSOS-4P Orbital shaker (Oxford, Connecticut, USA). Cell densities were determined by direct counting with a Neubauer chamber and an optical microscope Leica DM1000 LED (Wetzlar, Hesse, Germany). The required volumes of microalgae for feeding were taken directly from the culture flasks with a pipette, during its exponential phase, and added to the vessels with the copepods.

Nauplius size measurements

In preparation for the experiment, three months before, three separate populations of A. spartinus were conditioned in climatic chambers under specific culture conditions corresponding to three temperature treatments: 16, 20 and 24 °C. From each conditioned monoculture, 100 gravid females were carefully selected and placed in three 100 ml beakers. After a period of 12 hours, the adult females were removed, leaving the nauplii for further observation and measurement.

Then, nauplii (± 12 h) from each 100 ml beaker were divided into two 250 ml beakers per treatment, between 5 and 10 nauplii were randomly taken every 4 h, three to four times a day. Except, for the first hours, measurements were taken from a new cohort at 0, 2, 4, 6 and 9 h for 24 °C, and 0, 2, 4 and 8 h for 16 and 20 °C. For each measurement time, individuals were fixed with a 5% formalin solution for subsequent measurement.

In the case of the 16 °C treatment, two additional cohorts were obtained, because the total population of the first cohort was measured until day 14. A few copepodites appeared from day 10 onwards. Therefore, in order to describe the maximum possible period of nauplii life span, a second cohort was measured once a day from day 15 to 20 and every two days from day 22 to 34. In all cases, no dead specimens were measured.

The determination of naupliar sub-stages was compared to the work of Czaika (1982) and the pictorial key of Miracle (2015), according to the following simplified criteria: N1, rounded, newly hatched, presence of two antennules, antennas and mandibles, absence of forming or complete appendages in the ventral zone; N2, rounded with a slight drop shape, presence of two point-shaped appendages in the ventral zone; N3, drop shape, presence of two triple-pointed appendages in the ventral zone; N4, elongate fusiform posteriorly, presence of two maxillule exopods; N5, elongate fusiform posteriorly, presence of rudiments of the first swimming appendage; N6, elongate fusiform posteriorly, presence of rudiments of the first two swimming appendages.

Morphometric measurements were performed on the length and width for each naupliar stage. A Leica DM1000 microscope with DFC290 HD CMOS image capture (Wetzlar, Hesse, Germany) and Leica Application Suite V.4.10.0 software was used. Kruskal-Wallis analysis was used to determine differences in width and length between treatments.

Determination of nauplii survival to cold shock

Complementary to the previous experiment, the expected stunting of individual growth was evaluated for live feed preservation purposes. To that end, hatched nauplii were harvested at 24 °C using 45 and 150 µm mesh to separate them from other stages, some unwanted stages were removed until only nauplii remained and were stored at 16 °C pooled in four 500 ml beakers and fed with Tetraselmis sp. Nauplii were counted in five aliquot replicates of 2 ml to assess survival and were randomly measured (N = 36), to determine the normal distribution of naupliar size hatched at 24 °C and kept for nine days at 16 °C. The frequency of the data was standardised to a density function of a normal distribution to observe the trend.

Growth models

Software R-CRAN version 4.3.0 was used to calculate the parameters from growth rates, growth models as Linear, von Bertalanffy and Gompertz and growth rate-dependent models as allometric, complex allometric and Arrhenius. In all cases we use linear (lm) and nonlinear functions (nls). Akaike information criterion (AIC) values were used to compare models.

(Equation 1)

$$Growthrate=\frac{\left(L_{i+1}\right)-\left(L_i\right)}{\left(t_{i+1}\right)-\left(t_i\right)}$$

Where L_i: average prosome length (µm) nauplii stage from N1 to N6 and t_i: average time interval of each nauplii stage from t1 to t6.

For three temperatures (16, 20 and 24 °C), the relationship between prosome length and age of A. spartinus was described using a linear model, the von Bertalanffy growth function (von Bertalanffy, 1938) and Gompertz growth function (Gompertz, 1825) modified by de Mello et al. (2015), where the equations are described as follows:

Linear model:

(Equation 2)

$$L_t=bt+\mathrm{}\mathrm{a}$$

Where L_t: expected length (µm) at age t, a: intercept value, b: slope value and t: age in hours.

von Bertalanffy model:

(Equation 3)

$$L_t=L_{\mathrm{\infty }}\left(1-{exp}^{-k\left(t-t_o\right)}\right)$$

Where L_t: expected length (µm) at age t, L_∞: asymptotic length (µm), k: growth rate (day^-1) and t₀: theoretical age at which size is zero.

(Equation 4)

$$L_t=L_{\mathrm{\infty }}\left(1-{exp}^{-k*T_{corr}\left(t-t_o\right)}\right)$$

For the adjustment of the model, the asymptotic length L_∞ was set at a referential value of 280 µm.

T_corr, on the other hand, depends on the Arrhenius temperature (T_A) and may be approximated as follows, according to Kooijman (2010):

(Equation 5)

$$T_{corr}=\left(\exp \left\{\frac{T_A}{T_{ref}}-\frac{T_A}{T}\right\}\right)\mathrm{}$$

Where T_corr is the correction temperature (°K), T_A is the Arrhenius temperature (°K), T_ref is the reference temperature (°K) and T is the absolute temperature at which growth will be monitored (°K), (Kooijman, 2009).

Gompertz model:

(Equation 6)

$$L_t=a{exp}^{-b{exp}^{t-c}}$$

(taken from Mello et al., 2015)

Where L_t: expected length (µm) at age t, a: asymptotic value, b: constant rate of exponential growth, t: age in hours and c: age at inflection point.

The influence of temperature on growth rates was determined by a graph of a linear model, where the Arrhenius temperature (TA) is equal to the value of the graph slope, having as Y axis to the natural logarithm of the growth rate (LnØ) and as the X axis to the inverse value of the temperature (Kelvin degrees, 1/T) (van der Meer et al., 2006), whose equation would be as follows:

(Equation 7)

$$\mathrm{Ln}\left(\varnothing \right)=\left(T_A\right)(1/T)+LnA$$

Bělehrádek model:

The allometric function was performed between the physiological rate and temperature, which originally expressed as follows:

(Equation 8)

$$R={a(T-\alpha )}^b+e$$

Where 𝛼: simple index for temperature adaptation, linearly correlated with the environmental temperature. Nevertheless, in the present study, A. spartinus was grown under controlled thermal conditions (± 1 °C). Consequently, the modification of Heip (1974) was used, where a value of α = 0 is assumed, leaving the equation modified as follows:

(Equation 9)

$$R={aT}^b+e\mathrm{}$$

To develop this equation a linear model was carried out. We determined the influence of temperature on growth rates by a graph of a linear model, where the natural logarithm of the growth rate (Y axis) and the value of the temperature (X axis) whose equation would be as follows.

(Equation 10)

$$LnR=Lna+bLnT+e$$

Also, the complex allometric function was performed, which is expressed as follows.

(Equation 11)

$$R={aT}^{(b+clogT)}$$

We determined a linearised model that is quadratic in temperature that is called the exponential-quadratic model:

(Equation 12)

$$LnR=Lna+bLnT+c{\left(LnT\right)}^2+e\mathrm{}$$

Where R is the growth rate, T (°C) is the temperature at which growth was monitored, a, b, and c are constants for the allometric and the complex allometric models, e indicates error.

Akaike information criterion (AIC):

The AIC is a quantitative approach used to assess the degree of concordance between a model and the data it was derived from. Optimal models exhibit lower AIC values among them.

(Equation 13)

$$AIC=2k-2Ln\mathrm{L}̂$$

Where k is the number of independent variables used and L̂ is the maximised value of the likelihood function for the model (Akaike, 1974).

RESULTS

Individual growth of nauplii

A total of 811 measured nauplii were distributed in 360 for 16 °C, 214 for 20 °C, and 237 for 24 °C. The average sizes per temperature, length × width, of newly hatched nauplii were 96.03 ± 5.78 × 71.22 ± 7.28 µm, 99.47 ± 7.33 × 72.76 ± 6.03 µm and 94.84 ± 5.07 × 70.48 ± 7.0 µm corresponding to 16, 20 and 24 °C respectively. Lethargy in its life cycle in 16 °C-acclimatized cultures were reported.

The trend of lengths of nauplii per sub-stage were similar for 16 and 20 °C. However, at 24 °C a higher average growth in length was achieved (Fig. 1). Average growth ranges varied from 90 to 256 µm at 16 °C and 90 to 259 µm at 20 °C meanwhile at 24 °C varied from 90 to 276 µm.

Figure 1.
Average size by naupliar sub-stage of Apocyclops spartinus (bars indicate standard deviation, ns means statistically not significant and * means statistically significant among treatments).

The trend of widths of nauplii per sub-stage were similar for 16 and 20 °C. However, at 24 °C a higher average growth in width was achieved (Fig. 2). Average growth ranges varied from 75 to 140 µm at 16 °C and 75 to 136 µm at 20 °C meanwhile at 24 °C varied from 80 to 142 µm.

Figure 2.
Average width by naupliar sub-stage of Apocyclops spartinus (bars indicate standard deviation and * means statistically significant among treatments).

In this regard, the largest reported length and width of nauplii were 289 and 154 µm respectively at 16 °C. However, the largest average reported for length and width were 276 and 141 µm respectively at 24 °C (Fig. 1 and 2). These measurements indicate the specific size threshold close to 280 µm for nauplii before transitioning to copepodite, the subsequent developmental stage.

The average time of complete naupliar development was 100, 150, and 400 h for 24, 20 and 16 °C, respectively. The growth time also was similar in the three temperatures for the first two stages, with a growth range of 16 to 20 h for the N1 stage and between 40 to 64 h for N2, which is equivalent to 2 and 2.5 days for the three temperatures (Fig. 3). Metamorphosis to copepodite 1 of this species minimum occurred after 96 h at 24 °C.

Figure 3.
Average duration in hours per naupliar sub-stage of Apocyclops spartinus (bars indicate minimum and maximum).

It is important to note that the copepodite 1, at 16 °C was recorded sparsely between day 10^th (244 h) and 13^th (312 h), but regularly from day 14^th (328 h). However, some nauplii did not undergo metamorphosis at this temperature.

Nauplii survival

Survival (Fig. 4) of A. spartinus nauplii hatched at 24 °C and kept for nine days at 16 °C showed average initial densities ranging from 270 to 530 ind/2 ml.

Figure 4.
Mean values with standard error of number of Apocyclops spartinus nauplii / 2 ml preserved at 16 °C. Letters A, B, C and D indicate different samples.

While the modal progression of lengths affected by the temperature change (Fig. 5) showed a slight growth despite the cold stress. Day 9 was not considered in sample A, due to the limited data obtained.

Figure 5.
Normal distribution of naupliar size at 16 °C (dashed line: day 1; grey line: day 5 and black line: day 9). Letters A, B, C and D indicate different samples. The Y-axis represents the normal density function. In graph A, there is no line for day 9, due to the low number of individuals recorded.

Growth models

When evaluating growth models, we observed that all were highly significant (P < 0.001). The values of the Akaike information criterion (AIC) indexes, however, showed that the best model was Gompertz followed by Linear and finally von Bertalanffy for the naupliar period (Tab. 1).

Table 1.
Linear, von Bertalanffy, and Gompertz models of naupliar stage of Apocyclops spartinus (*** = P < 0.001).

Model	Parameter 1	Parameter 2	Intercept	Sig.	AIC
	(St. error)	(St. error)	(St. error)
Linear 16 °C	b: 0.388 (0.012)		a: 118.819 (2.74)	***	3539.44
Linear 20 °C	b: 1.202 (0.017)		a: 91.323 (1.52)	***	1717.512
Linear 24 °C	b: 1.764 (0.039)		a: 104.758 (2.18)	***	2115.695
von Bertalanffy 16 °C	k: 45.19 (1.194)		t0: -0.0075 (0.00044)	***	3255.619
von Bertalanffy 20 °C	k: 91.12 (2.985)		t0: -0.0035 (0.00026)	***	1932.919
von Bertalanffy 24 °C	k: 142.5 (5.448)		t0: -0.0029 (0.0002)	***	2217.784
Gompertz 16 °C	a: 282 (4.609)	b: 0.007646 (0.00039)	c: 21.88 (2.832)	***	3202.603
Gompertz 20 °C	a: 691.2 (107.3)	b: 0.005095 (0.00062)	c: 134.5 (30.48)	***	1697.678
Gompertz 24 °C	a: 780.9 (280.1)	b: 0.00677 (0.0017)	c: 101.2 (51.51)	***	2110.474

In the Gompertz model, the growth constant (c) increased sixfold with increasing 4 °C, but increased fivefold with increasing 8 °C. This model was sensitive to how the increase in growth rates is related to temperature, with a tendency to stabilise the slope at 24 °C. The von Bertalanffy’s growth constant (k) doubled with increasing 4 °C and tripled with increasing 8 °C, this continual increase shows a direct relationship of individual growth with temperature.

In the linear model, the slope tripled with an increase of 4 °C and quadrupled with an increase of 8 °C, and the trend of growth rates from the beginning remained upward until the change from stage N4 to N5 where it decreased. The lowest rate was nevertheless observed at 16 °C between the first N1 and N2 stages. While at 20 °C the minimum was observed between stages N2 and N3. Thus at 24 °C the minimum was between stages N4 to N5. The reduction in rates was also observed between stages N6 and C1, except for 20 °C (Tab. 3). In all temperature cases, the linear models were found to be significant, but with the worst value of the Akaike index at 16 °C.

While evaluating the growth rate-dependent models, we can observe that the allometric complex model was not significant and it showed the worst adjustment, in this case, it did not predict the individual growth for A. spartinus at least within the temperature range tested, meanwhile the Arrhenius model was slightly better supported than the simple allometric model, both were the best fitted models (Tab. 2).

Table 2.
Simple and complex Allometric and Arrhenius Models of growth rates from naupliar stage of Apocyclops spartinus (* = P < 0.05). The temperature correction is at the end of the table.

Model	Parameter 1	Parameter 2	Intercept	Sig.	AIC
	(St. error)	(St. error)	(St. error)
Allometric simple	0.17525 (0.0338)		-3.53791 (0.68340)	*	320.863
(16, 20 and 24 °C)
Allometric complex	0.486637 (0.6023)	-0.00779 (0.0150)	-6.568695 (5.894567)		422.531
(16, 20 and 24 °C)
Arrhenius	15069.27 (2892.78)		51.38 (9.87)	*	320.814
(16, 20 and 24 °C)
Temperature correction Function	Tcorr. (24 °C) = 1.000 Tcorr. (20 °C) = 0.501 Tcorr. (16 °C) = 0.246

Table 3.
Growth rates from N1 to C1 at three temperatures. Where, N = Nauplius and C = Copepodite.

	Growth Rates (µm/hours)
Stages	16 °C	20 °C	24 °C
N1 - N2	0.244	0.986	1.509
N2 - N3	0.611	0.416	1.749
N3 - N4	0.531	1.560	1.995
N4 - N5	0.469	1.514	1.273
N5 - N6	0.558	1.327	3.425
N6 - C1	0.057	1.022	0.205

DISCUSSION

In the present study, significant adaptive thermal differences were observed among naupliar size and width per stages of A. spartinus at 24, 20 and 16 ºC, except among N1 sizes, and high mortalities at cold shock. Maximum length and width were observed at 24 °C, contrary to classical adaptive plasticity theories for ectotherms, in which slow development in cold environments increase size (Angilletta et al., 2004).

The average lifespan of the N6 stage increased from 96 h (up to 112 h) at 24 °C, towards 400 h (up to 672 h) at 16 °C, this affected proportionally the generational time in acclimatized cultures. Pan et al. (2017) compared four acclimatized generations of A. royi, at 18 and 28 ºC in 20 PSU salinity, and they found at lower temperature a trend of size increase in females, decreased nauplii size, increased nauplii production and progressive decrease in fatty acids, omega-6 and omega-3. Nevertheless, they did not conclude a relationship between temperature, size, and the accumulation of fatty acids.

Selective breeding of individual animals with higher productivity, commonly related to greater size or volume (Gillooly et al., 2002), is often evident. Nonetheless, in the case of micro-invertebrates such as copepods, it can be estimated through the populations best adapted to temperature or feeding changes (Farhadian et al., 2008), as well as, the evaluation of their potentialities such as temperature-based egg hatching rate (Hansen et al., 2010), morphological (Souissi et al., 2016), biochemical (Rayner et al., 2015), and genetic (Amparyup et al., 2022) changes. In our case, direct measurements on an individual basis, allowed us to model thermal responses according to metabolic theories, as these are usually calculated with indirect based weight-based measurements (Forster et al., 2011).

Gómez-Gutiérrez et al. (1999) reported a case where the specific growth rates of P. parvus, C. furcatus, and A. clausi, based on micrograms of carbon (μg C), were not associated with food availability or temperature; a phenomenon attributed to seasonal reproductive cycles. Hopcroft and Roff (1998) also observed a slower nauplii growth of cyclopoids regarding calanoids in a microcosm incubation, showing a significant relationship between size and instantaneous growth rates, based on weight (g). It was suggested that there was a greater influence of temperature on nauplii growth rather than on feeding. Our experiments under laboratory conditions show nauplii growth rates based on µm h^-1 were affected particularly by each temperature, with a constant decrease before nauplius-copepodite metamorphosis. This pattern of development under optimal conditions provides a useful starting point for further conditions.

An analogy of copepod growth rate variation by stage of the moult cycle with linear growth of decapod zoea larvae, with ad libitum feeding, was drawn by Miller (2008). It was suggested that first instars are faster than the later ones, independent of food. This time interval difference is assumed to be because of the process of exoskeleton morphogenesis, which is a process that becomes more complex as the organism develops. Although our linear model with A. spartinus was significant, it obtained the lowest value of the Akaike index at 16 °C, pointing out that linearity could explain the process of exoskeleton morphogenesis but non-linear models are necessary to get better adjustment. We found at 16 °C, a large number of dead N6 stage nauplii with oil droplets that were unable to reach the C1 stage. For that reason, it is considered that the association of exoskeleton morphogenesis with the "Point of Reserve Saturation - PRS”, defined as the time when enough reserves are accumulated for a successful instar without food (Anger and Dawirs, 1981), is not only inherent to feeding (Crain and Miller, 2001), but also to the quality of water, considering optimal values of temperature, salinity or oxygen levels (Zeng et al., 2020).

This biological association limits the nauplii growth to a model with a mandatory threshold, either asymptotic or logistic-type as the von Bertalanffy or Gompertz model assumes, respectively. Both models are commonly used due to their sensitivity to rapid initial growth, characteristic of micro-crustaceans and also widely used with fishes (Hernández-Llamas and Ratkowsky, 2004).

The von Bertalanffy is the most studied, friendly, and applied growth model, which produces asymptotic growth curves within the bounds of the infinite length parameter and expressed by a sensitive k parameter (Rumi et al., 2007). This has drawbacks in certain cases, because it can be applied incorrectly to describe the growth of non-asymptotic marine species like cartilaginous fishes (Cailliet et al., 2006) or some cephalopods (Goicochea-Vigo et al., 2019). In contrast, in our study, the A. spartinus nauplii curve was limited by a maximum length near to 280 µm. Jager et al. (2017) used this model for bioenergetics purposes based on measurements of nitrogen (N) and carbon (C), and explained a truncated curve due to the maximum growth of adults. Our direct measurements, however, were reliable and precise, because of the level of detail obtained in our data and the number of samples. This model was proportional to the temperature increase.

The Gompertz’s growth model is an asymmetrical equation with three parameters corresponding to the upper asymptote, time origin, and rate constant, widely used as a response to biological processes (Winsor, 1932). Kiørboe et al. (2015) used Gompertz functions to explain copepod survival, due to mortality rate increasing monotonously with age. In our case, this model exhibited a tendency to stabilize the slope at 24 °C and it was sensitive to the relationship between temperature and the increase in growth rates. It is assumed that this sigmoidal model is better adapted to the larval development of bivalves or fishes (Urban, 2002; Watanabe and Kuroki, 1997). In our case, the maximum growth rate increased between naupliar stage N5 and N6 at 24 °C (Tab. 3), unlike the two lower temperatures. Which also can be interpreted as a physiological response to an optimal range under laboratory conditions. This threshold explained a better development temperature prior to the morphological changes brought about by metamorphosis, similar to the results of Dahms (1992), who stated that in every development of the sub-naupliar stage, one set of structures changed and another remained latent, affecting the growth rate in the N6 prior to C1.

Slight differences were observed between the Arrhenius and the simple allometric model (Tab. 2), which reflects the behavior of A. spartinus in optimal culture conditions (24 °C) towards hypothermic stress conditions (20 and 16 °C). This range corresponds to the climate under Non-ENSO (El Niño-Southern Oscillation) weather conditions for the wetlands of the central Peruvian coast (Vizcardo and Gil-Kodaka, 2015), which are the natural habitat for this strain. This high Arrhenius temperature (TA = 15069.27 K) compared with other animals enables us to support the idea that, this species has a restricted distribution to environments with stable temperature. The Arrhenius temperature nevertheless can thus change with stages in some species (Kooijman, 2009) and it begs the question, how the correction temperature would change if we increased the temperature from 28 to 32 °C to simulate ENSO conditions.

The modification of Bělehrádek's simple allometric model proposed by Heip (1974) was used in our experiment, and it reduced from three to two parameters using the copepod Tachidius discipes Giesbrecht, 1881, as a basis to explain its development based on temperature. In addition, Palmer and Coull (1980) explained that the curvilinearity of this model decreases when a critical maximum temperature is reached. In the present study, the simple allometric model was used to evaluate the adaptability of the growth of A. spartinus nauplii within an interval below its optimum developmental temperature. Despite this, a significant relationship was observed.

It is important to emphasize the conservation of Peruvian coastal wetlands, because these environments become important for provisioning ecosystem services by offering new potential aquaculture resources. Therefore, emphasis should be placed on restoring habitats (Sarkar et al., 2020), and allowing us to face physical and chemical impacts in Ventanilla wetlands and along the interconnected network of coastal wetlands of Peru (Gómez et al., 2023).

In conclusion, according to the observed naupliar sizes reached under laboratory conditions, A. spartinus from the central coast of Peru has a potential to be used as live food for marine fish larvae culture, especially for larvae whose mouths are smaller than 200 µm, a size suggested by Raheem et al. (2021), Hyndes et al. (1997), and Knutsen and Tilseth (1985) or about 13% of the mouth gape (Swalethorp et al., 2015). In acclimatized copepods, decreasing temperature lengthened the growing time from 24 to 20 ºC (1.75 times) and from 20 to 16 ºC (4 times). Growth rates were affected over the temperature range evaluated, but all decreased before nauplius-copepodite metamorphosis. These rates allowed us to evaluate the pattern of development under optimal conditions and to differentiate them from other non-thermal treatments or environmental conditions. Five out of six different models were significant and they explained A. spartinus’ performance during these early stages. Gompertz was the best growth model according to Akaike’s criterion, while growth rate-dependent models showed that Arrhenius and simple Allometric models were the best. Cold shock at 16 ºC was tested in non-acclimated strains, and delayed naupliar growth, but with high mortalities. These results of copepod adaptations are useful in aquaculture management; in particular, to achieve a broodstock culture at 24 °C and once the eggs have hatched, the temperature could be gradually decreased to 20 °C, but not as far as 16 °C, to harvest specific naupliar sizes. Extending the period of copepod nauplii would guarantee a consistent provision of appropriately sized live food for the initial larval feeding. It is essential to highlight those mathematical modelling responses of this copepod are based on their diet of Tetraselmis sp. This approach encourages the application of these mathematical models to various dietary regimes, thereby expanding our understanding of their efficacy and adaptability across different nutritional contexts. The cultivation conditions for microalgae are standardized (as detailed in the microalgae culture section), ensuring that the nutritional quality of the feed remains stable and consistent, with harvests consistently occurring during the exponential growth phase.

ACKNOWLEDGEMENTS

This research was financially supported by Instituto del Mar del Perú. The authors wish to thanks the BGOA professional staff and the anonymous reviewers for their careful reading of our manuscript and their many insightful comments and suggestions.

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• SUPPLEMENTARY MATERIAL
  The evidence and data that support the findings of this study are available from the corresponding author upon reasonable request. The measurement data for each temperature was uploaded to the Mendeley Data repository (https://doi.org/10.17632/j87d6z84ts.1).
• Consent for publication
  All authors have read and agreed to the published version of the manuscript.
• Funding
  Research was partially funded by the Ministry of Production-IMARPE-DGIA (PpR Budget program 0094 “Ordenamiento y Desarrollo de la Acuicultura”). The specimens analysed are property of the BGOA of the IMARPE.
• Study association
  This work is part of the Master’s Thesis of the first author in the Programa de Maestría en Ecosistemas y Recursos Acuáticos, Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos (MERA-UNMSM).

Edited by

• Associate Editor:
  Fabiano Paschoal

• Editor-in-chief
  Christopher Tudge

Data availability

The evidence and data that support the findings of this study are available from the corresponding author upon reasonable request. The measurement data for each temperature was uploaded to the Mendeley Data repository (https://doi.org/10.17632/j87d6z84ts.1).

Publication Dates

• Publication in this collection
  03 Feb 2025
• Date of issue
  2025

History

• Received
  18 Dec 2023
• Accepted
  15 Sept 2024