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Shelter preference and variation in the daily activity pattern of the ornamental shrimp Neocaridina davidi (Caridea: Atyidae)

Abstract

Neocaridina davidi (Bouvier, 1904) is a shrimp commonly used in aquaculture throughout the world. It is an exotic species in several places. We investigated the preference of N. davidi for four types of shelter (rock, Vesicularia sp., Egeria sp., and wood) and its nictemeral activity variation. Individuals were divided into three experimental groups: males, non-ovigerous females, and ovigerous females. They were placed in tanks with the four shelter types and observed every 3 hours for 72 hours. Neocaridina davidi presented cryptic behavior with 82.1 ± 8.69% of individuals sheltering per observation. Sheltering was higher during the daytime (88.8 ±5.54%) than at nighttime (75.4 ± 5.53%). Vesicularia sp. was the most used shelter followed by wood. The least used shelter type was a rock. Swimming and walking were more frequently observed at nighttime, especially for ovigerous females. We have demonstrated the importance of providing shelter for the maintenance of N. davidi in tanks as well as its higher activity at nighttime.

Keywords
Aquarium trade; aquaculture; behavioral experiments; circadian rhythm; red cherry

INTRODUCTION

The shrimp Neocaridina davidi (Bouvier, 1904) belongs to the family Atyidae and is native to China, Korean Peninsula, Taiwan, and Vietnam. It is broadly used in the aquarium trade throughout the world and is an exotic species in several locations outside its native distribution range (Cai, 1996Cai Y 1996. A revision of the genus Neocaridina (Crustacea, Decapoda, Atyidae). Acta Zootaxonomica Sinica, 21(2): 129-160.; Liang, 2004Liang XQ 2004. Fauna Sinica. Invertebrata: Crustacea: Decapoda: Atyidae. Science Press, Beijing, China, 375p.; Wowor et al., 2004Wowor D, Cai Y and Ng PKL 2004. Crustacean: Decapoda: Caridea, p. 337-357. In: C Yule and HS Yong (eds), The Freshwater Invertebrates of Malaysia and Singapore. Malaysian Academy of Sciences.; Klotz et al., 2013Klotz W, Miesen FW, Hullen S and Herder F 2013. Two Asian freshwater shrimp species found in a thermally polluted stream system in North Rhine-Westphalia, Germany. Aquatic Invasions, 8(3): 333-339. http://dx.doi.org/10.3391/ai.2013.8.3.09
http://dx.doi.org/10.3391/ai.2013.8.3.09...
; Mitsugi and Suzuki, 2018Mitsugi M and Suzuki H 2018. Life history of an invasive freshwater shrimp Neocaridina davidi (Bouvier, 1904), (Decapoda: Caridea: Atyidae) in the Tomoe River, the Boso Peninsula, eastern Japan. Crustacean Research, 47: 9-16. https://doi.org/10.18353/crustacea.47.0_9
https://doi.org/10.18353/crustacea.47.0_...
; Jablońska et al., 2018Jablonska A, Mamos T, Gruska P, Szlauer-Lukaszewska A and Grabowski M 2018. First record and DNA barcodes of the aquarium shrimp, Neocaridina davidi, in Central Europe from thermally polluted River Oder canal, Poland. Knowledge and Management of Aquatic Ecosystems, 419(14): 1-5. https://doi.org/10.1051/kmae/2018004
https://doi.org/10.1051/kmae/2018004...
; Schoolman and Arndt, 2018Schoolmann G and Arndt H 2018. Population dynamics of the invasive freshwater shrimp Neocaridina davidi in the thermally polluted Gillbach stream (North Rhine-Westphalia, Germany). Limnologica, 71: 1-7. https://doi.org/10.1016/j.limno.2018.05.001
https://doi.org/10.1016/j.limno.2018.05....
). Its relatively small size and noticeable coloration are among the most attractive attributes related to its use by aquarists (Pantaleão et al., 2015Pantaleão JAF, Barros-Alves SP, Tropea C, Alves DFR, Negreiros-Fransozo ML and López-Greco LS 2015. Nutritional vulnerability in early stages of the freshwater ornamental red cherry shrimp. Neocaridina davidi (Bouvier, 1904) (Caridea: Atyidae). Journal of Crustacean Biology, 35(5): 676-681. https://doi.org/10.1163/1937240X-00002357
https://doi.org/10.1163/1937240X-0000235...
).

Neocaridina davidi has been studied in recent years regarding its basic biology and improvement of culture conditions. There has been a special focus on post-embryonic development, effects of starvation, presence of biofilm and population density on growth and reproduction (Pantaleão et al., 2015Pantaleão JAF, Barros-Alves SP, Tropea C, Alves DFR, Negreiros-Fransozo ML and López-Greco LS 2015. Nutritional vulnerability in early stages of the freshwater ornamental red cherry shrimp. Neocaridina davidi (Bouvier, 1904) (Caridea: Atyidae). Journal of Crustacean Biology, 35(5): 676-681. https://doi.org/10.1163/1937240X-00002357
https://doi.org/10.1163/1937240X-0000235...
; 2017Pantaleão JAF, Gregati RA, Costa RC, López‐Greco LS and Negreiros‐Fransozo ML 2017. Post‐hatching development of the ornamental ‘Red Cherry Shrimp’ Neocaridina davidi (Bouvier, 1904) (Crustacea, Caridea, Atyidae) under laboratorial conditions. Aquaculture Research, 48(2): 553-569. https://doi.org/10.1111/are.12903
https://doi.org/10.1111/are.12903...
; Wlodarczyk et al., 2017Włodarczyk A, Sonakowska L, Kamińska K, Marchewka A, Wilczek G, Wilczek P, Student S and Rost-Roszkowska M 2017. The effect of starvation and re-feeding on mitochondrial potential in the midgut ofNeocaridina davidi(Crustacea, Malacostraca). PLoS ONE, 12(3): e0173563. https://doi.org/10.1371/journal.pone.0173563
https://doi.org/10.1371/journal.pone.017...
; 2019Włodarczyk A, Wilczek G, Wilczek P, Student S, Ostróżka A, Tarnawska M and Rost-Roszkowska M 2019. Relationship between ROS production, MnSOD activation and periods of fasting and re-feeding in freshwater shrimpNeocaridina davidi(Crustacea, Malacostraca).PeerJ, 7: e7399. https://doi.org/10.7717/peerj.7399
https://doi.org/10.7717/peerj.7399...
). Recently Tomas et al. (2020Tomas AL, Sganga DE and Lopez Greco LS 2020. Effect of background color and shelters on female pigmentation in the ornamental red cherry shrimp Neocaridina davidi (Caridea, Atyidae).Journal of the World Aquaculture Society, 51(3): 775-787. https://doi.org/10.1111/jwas.12660
https://doi.org/10.1111/jwas.12660...
) have demonstrated the influence of color substrate on coloration of female individuals. No studies have yet focused on daily activity rhythm.

Shelters are valuable resources for crustaceans as they act as a defense against predators, lower the risk of cannibalism, and attract sexual partners (Marshall et al., 2005Marshall S, Warburton K, Paterson B and Mann D 2005. Cannibalism in juvenile blue-swimmer crabs Portunus pelagicus (Linnaeus, 1766): effects of body size, moult stage and refuge availability. Applied Animal Behaviour Science, 90(1): 65-82. https://doi.org/10.1016/j.applanim.2004.07.007
https://doi.org/10.1016/j.applanim.2004....
; Edwards and Herberholtz, 2005Edwards DH and Herberholz J 2005. Crustacean models of aggression, p. 38-61. In: RJ Nelson (Ed.), Biology of aggression. Oxford, UK, Oxford University Press. 528p.). Shelter type can influence survivorship and harvested biomass of cultivated species (Jones and Ruscoe, 2001Jones CM and Ruscoe IM 2001. Assessment of Five Shelter Types in the Production of Redclaw Crayfish Cherax quadricarinatus (Decapoda: Parastacidae) Under Earthen Pond Conditions. Journal of the World Aquaculture Society, 32(1): 41-52. https://doi.org/10.1111/j.1749-7345.2001.tb00920.x
https://doi.org/10.1111/j.1749-7345.2001...
). Shelters with higher structural complexity tend to be more attractive to shrimps as they provided more individualized spaces for animals to hide (Park et al., 2015Park KY, Park HG and Kwon ON 2015. Effects of stocking density and shelter type on the growth and survival of pandalid shrimp (Pandalopsis japonica Balss, 1914) juveniles.Crustaceana, 88(2): 144-151. https://doi.org/10.1163/15685403-00003407
https://doi.org/10.1163/15685403-0000340...
). Decapod crustaceans are sensitive to stress (Elwood et al., 2009Elwood RW, Barr S and Patterson L 2009. Pain and stress in crustaceans? Applied Animal Behaviour Science, 118(3-4): 128-136. https://doi.org/10.1016/j.applanim.2009.02.018
https://doi.org/10.1016/j.applanim.2009....
; Elwood, 2012Elwood RW 2012. Evidence for pain in decapod crustaceans. Animal Welfare, 21(1): 23-27. https://doi.org/10.7120/096272812X13353700593365
https://doi.org/10.7120/096272812X133537...
; Magee and Elwood, 2013Magee B and Elwood RW 2013. Shock avoidance by discrimination learning in the shore crab (Carcinus maenas) is consistent with a key criterion for pain. Journal of Experimental Biology, 216(3): 353-358. https://doi.org/10.1242/jeb.072041
https://doi.org/10.1242/jeb.072041...
; Fossat et al., 2014Fossat P, Bacqué-Cazenave J, De Deurwaerdère P, Delbecque JP and Cattaert D 2014. Anxiety-like behavior in crayfish is controlled by serotonin.Science, 344(6189): 1293-1297. https://doi.org/10.1126/science.1248811
https://doi.org/10.1126/science.1248811...
), so creating a more pleasant environment by providing shelter could improve living conditions.

Shrimp species show a variation in their activity pattern throughout the day, being more active at night. This pattern has been reported for caridean species such as Palaemon xiphias Risso, 1818 (Guerao, 1995Guerao G 1995. Locomotor activity patterns and feeding habits in the prawn Palaemonxiphias (Crustacea: Decapoda: Palaemonidae) in Alfacs Bay, Ebro Delta (northwest Mediterranean). Marine Biology, 122: 115-119. https://doi.org/10.1007/BF00349284
https://doi.org/10.1007/BF00349284...
), Palaemon serratus (Pennant, 1777) (Guerao and Ribera, 1996Guerao G and Ribera C 1996. Locomotor activity patterns and feeding habits in the prawnPalaemon serratus(Pennant, 1777) (Decapoda, Palaemonidae) in the Alfa Bay, Elbro Delta, Spain.Crustaceana, 69(1): 101-112. ), Processa edulis (Risso, 1816), and Palaemon adspersus Rathke, 1837 (Guerrao and Abelló, 1996Guerao G and Abelló P 1996. Patterns of activity in the sympatric prawns Palaemon adspersus and Processa edulis (Decapoda, Caridea) from a shallow Mediterranean bay. Scientia Marina, 60(2-3): 319-324.), as well as for Dendrobranchiata species such as Penaeus monodon Fabricius, 1798, Penaeus semisulcatus De Haan, 1844 (Moller and Jones, 1975Moller TH and Jones DA 1975. Locomotory rhythms and burrowing habits of Penaeus semisulcatus (de Haan) and P. monodon (Fabricius) (Crustacea: Penaeidae).Journal of Experimental Marine Biology and Ecology, 18(1): 61-77. https://doi.org/10.1016/0022-0981(75)90017-9
https://doi.org/10.1016/0022-0981(75)900...
), Solenocera membranacea (Risso, 1816) (see Aguzzi et al., 2006Aguzzi J, Abelló P and García JA 2006. Daily activity patterns of the mud shrimp Solenocera membranacea (Decapoda: Penaeoidea: Solenoceridae) in the western Mediterranean: a Comparison by Depth and Season.Bulletin of Marine Science, 79(2): 353-364.), and Artemesia longinaris Spence Bate, 1888 (see Carvalho-Batista et al., 2012Carvalho-Batista A, Castilho AL, Fransozo A and Costa RC 2012. Diel comparison of the catch and size of the shrimp Artemesia longinaris (Dendrobranchiata, Penaeidae) in the Ubatuba region, northern coast of the state of São Paulo.Crustaceana, 85(10): 1179-1191. https://doi.org/10.1163/15685403-00003122
https://doi.org/10.1163/15685403-0000312...
). Understanding the circadian rhythm of a cultivated species can improve its management by adjusting the feeding time to when animals are more active (Santos et al., 2016Santos ADA, López-Olmeda JF, Sánchez-Vázquez FJ and Fortes-Silva R 2016. Synchronization to light and mealtime of the circadian rhythms of self-feeding behavior and locomotor activity of white shrimps (Litopenaeus vannamei).Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 199: 54-61. https://doi.org/10.1016/j.cbpa.2016.05.001
https://doi.org/10.1016/j.cbpa.2016.05.0...
). Furthermore as N. davidi is widely utilized in the aquarium trade individuals of this species can be exposed to artificial light constantly. Artificial light at night can alter the behavior of some species of decapod crustaceans (Fisher et al., 2020Fischer JR, Gangloff MM and Creed RP 2020. The behavioral responses of 2 appalachian crayfish to cool and warm spectrum led lights at night.Freshwater Science, 39(1), 39-46. https://doi.org /10.1086/707459
https://doi.org /10.1086/707459...
), and the disruption of circadian cycle by the exposure to artificial light promote physiological alterations and increase the mortality rate (Fanjul-Moles et al., 1998Fanjul-Moles ML, Bosques-Tistler T, Prieto-Sagredo J, Castanón-Cervantes O and Fernández-Rivera-Rıo L 1998. Effect of variation in photoperiod and light intensity on oxygen consumption, lactate concentration and behavior in crayfish Procambarus clarkii and Procambarus digueti.Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 119(1), 263-269. https://doi.org/10.1016/S1095-6433(97)00413-3
https://doi.org/10.1016/S1095-6433(97)00...
; Farhadi and Jensen, 2016Farhadi A and Jensen MA 2016. Effects of photoperiod and stocking density on survival, growth and physiological responses of narrow clawed crayfish (Astacus leptodactylus).Aquaculture Research, 47(8): 2518-2527. https://doi.org/10.1111/are.12700
https://doi.org/10.1111/are.12700...
). So, the knowledge of their daily rhythm and how the species behaves each hour of the day is also essential to provide optimal conditions to these animals.

We investigate the preference of N. davidi for shelter type as well as their daily activity variation and shelter use. We hypothesize that individuals will use shelters during most of their daytime cycle and will prefer shelters with high structural complexity. We also hypothesize that most locomotion will happen during the nighttime.

MATERIAL AND METHODS

Animal acquisition and culture

The specimens were commercially acquired and transported to the laboratory where they were kept in tanks. They were fed twice a day with the commercial fish food TetraColor (TETRA; Tetra GmbH, Herrenteich, Germany) with the following approximate composition: 47.5% minimum crude protein, 6.5 % minimum crude fat, 2.0% maximum crude fiber, 6% max moisture, 1.5% minimum phosphorus, 100 mg.kg-1 minimum ascorbic acid (vit C), 8000 mg.kg-1 minimum omega 3-fatty acids. This diet was previously tested and has been considered adequate for culture of this species (Pantaleão et al., 2015Pantaleão JAF, Barros-Alves SP, Tropea C, Alves DFR, Negreiros-Fransozo ML and López-Greco LS 2015. Nutritional vulnerability in early stages of the freshwater ornamental red cherry shrimp. Neocaridina davidi (Bouvier, 1904) (Caridea: Atyidae). Journal of Crustacean Biology, 35(5): 676-681. https://doi.org/10.1163/1937240X-00002357
https://doi.org/10.1163/1937240X-0000235...
).

Shrimps were placed in three tanks 24 hours before the beginning of the experiments for acclimation. Tanks measuring 44 ( 20 ( 27 cm (length ( width ( height) with a 23-liter capacity were filled with filtered water and kept aerated with a pump, with constant light and temperature (23 °C). All material was cleaned between replicates; tanks and shelters were washed with treated running water to remove microorganisms that could have grown from previous experiments.

Sexing was based on macroscopic analysis of the following secondary sexual characters: presence (males) or absence (females) of the appendix masculina on the second pair of pleopods (Smith and Williams, 1980Smith MJ and Williams WD 1980. Infraspecific variations within the Atyidae: a study of morphological variation within a population of Paratya australiensis (Crustacea: Decapoda). Marine and Freshwater Research, 31(3): 397-407. https://doi.org/10.1071/MF9800397
https://doi.org/10.1071/MF9800397...
), and larger first pair of pleopods (males) (Pantaleão et al., 2017Pantaleão JAF, Gregati RA, Costa RC, López‐Greco LS and Negreiros‐Fransozo ML 2017. Post‐hatching development of the ornamental ‘Red Cherry Shrimp’ Neocaridina davidi (Bouvier, 1904) (Crustacea, Caridea, Atyidae) under laboratorial conditions. Aquaculture Research, 48(2): 553-569. https://doi.org/10.1111/are.12903
https://doi.org/10.1111/are.12903...
). Ovigerous females were those with embryos attached to the pleopods.

Experimental procedure

Shrimps were divided into three experimental groups: males, non-ovigerous females, and ovigerous females. Ten individuals from the same experimental group were placed together in each tank with four shelter types: 1) Java moss (Vesicularia sp.); 2) rock fragment; 3) Brazilian Waterweed (Egeria sp.); and 4) piece of wood. All shelters used in the experiments had a total surface area of approximately 250 cm² and were placed at least 5 cm apart (Fig. 1). Shelter areas were measured using the software ImageJ (Schneider et al., 2012Schneider CA, Rasband WS and Eliceiri KW 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9: 671-675. https://doi.org/10.1038/nmeth.2089
https://doi.org/10.1038/nmeth.2089...
). Shelter position was varied in the replicates to avoid placement effect (1 to 4) and preference for a specific side of the tank. Five consecutive replicates were made for each shrimp experimental group (totaling 5 tanks and 50 shrimps per group). All shrimps used in the experiments had their carapace length (CL) measured with a digital caliper (0.01 mm), and we attempted to minimize the size variation inside the groups by choosing individuals with similar CL to compose the groups. The carapace length varied from 3.04 to 3.68 mm (3.41 ± 0.28 mm) for males, 4.74 to 6.39 mm (5.44 ± 0.49 mm) for non-ovigerous females, and from 5.1 to 6.39mm (5.74 ± 0.64 mm) for ovigerous females.

Figure 1.
Representation of experimental tanks containing the four shelter types (Egeria sp., wood, Java moss, and rock) offered to Neocaridina davidi (Bouvier, 1904).

Animals were kept at a 12/12-hour light/dark cycle throughout the experiment. A white fluorescent light bulb (15 Watts) was used for the daytime phase while a red incandescent light bulb (15 Watts) was used for the nighttime observations (Rodriguez and Naylor, 1972Rodriguez G and Naylor E 1972. Behavioural rhythms in littoral prawns.Journal of Marine Biology Association, 52(1): 81-95. https://doi.org/10.1017/S0025315400018592
https://doi.org/10.1017/S002531540001859...
; Hindley, 1975Hindley JPR 1975. Effects of endogenous and some exogenous factors on the activity of juvenile banana prawnPenaeus merguiensis.Marine Biology, 29: 1-8. https://doi.org/10.1007/BF00395521
https://doi.org/10.1007/BF00395521...
; Scudder et al., 1981Scudder K, Pasanello E, Krafsur J and Ross K 1981. Analysis of locomotory activity in juvenile giant Malaysian prawns, Macrobrachium rosenbergii (De Man) (Decapoda, Palaemonidae). Crustaceana, 40(1): 31-35. ; Pontes, 2006). The room where the experiments were carried out is closed to prevent any light entry, so the only light available came from the light bulb. After acclimation, animals were observed for three consecutive days. Individual behaviors were evaluated by the focal animal method (adapted from Martin and Bateson, 1993Martin P, Bateson PPG and Bateson P 1993. Measuring behaviour: an introductory guide. Cambridge, Cambridge University Press. 246p.). The number of animals in shelters was recorded every two minutes for 20 minutes throughout pre-established observation periods, totaling 11 records per observation period. We established eight observation periods in a 24-hour period (adapted from Freire et al., 2011): four periods in at daytime (7am: 07:00 - 07:20am; 10am: 10:00 - 10:20am; 1pm: 1:00 - 1:20pm; 4pm: 4:00 - 4:20pm) and four at nighttime (7pm: 7:00 - 7:20pm; 10pm: 10:00 - 10:20pm; 1am: 1:00 - 1:20am; 4am: 4:00 - 4:20am). The number of individuals not using shelters and animals walking or swimming was also recorded during the observations to investigate the daily activity pattern for the species (Fig. 2). Animals were not fed throughout the experiment.

Figure 2.
Recorded behaviors of Neocaridina davidi (Bouvier, 1904) during the observation periods.

Characterization of shelters and degree of complexity

The degree of complexity of each shelter was defined according to its architecture (Beukers and Jones, 1998), for example, if the structure of a shelter allows a shrimp to enter its interior, the degree of complexity of that specific shelter is considered high. And if the structure of a shelter is simple, with little branching and making it impossible for the shrimp to hide completely, the degree of complexity of this shelter is considered low.

Among the four shelters used in the present study, the ones with the highest degree of complexity were wood and Java moss, while Egeria sp. and rock were the shelters with the least complexity. Both the wood, and especially the Java moss, had openings that allowed the shrimp to enter their interior, either partially (wood) or fully (Java moss). The branches of Java moss float in the water column, creating numerous small openings that the shrimps could access while remaining hidden within the moss. The wood fragments had small cracks allowing a limited number of shrimps to hide. On the other hand, Egeria sp. and the rocks have a simpler architecture, not having many branches or crevices where these shrimps could enter and be hidden, so they were considered shelters with low structural complexity.

Beyond the difference in complexity level the shelters were chosen due to their popularity with aquarists and because they can be easily found and used by shrimp keepers. Plants of the genus Egeria are very common in Brazil and very popular in aquarium trade (Negrisoli et al., 2003Negrisoli E, Martins D, Velini DE and Ferrera WLB 2003. Degradação de diquat em condições de caixa d'água com e sem plantas de egéria.Planta Daninha, 21: 93-98. https://doi.org/10.1590/S0100-83582003000400014
https://doi.org/10.1590/S0100-8358200300...
; Lorenzi, 2008Lorenzi H 2008. Plantas daninhas do Brasil: terrestres, aquáticas, parasitas e tóxicas. 4ª ed., Nova Odessa, Instituto Plantarum, 640p.), wood and rock are used by many aquarists to ornament tanks. Moreover, Java moss has already been used as a shelter in experiments with N. davidi (Tomas et al., 2020Tomas AL, Sganga DE and Lopez Greco LS 2020. Effect of background color and shelters on female pigmentation in the ornamental red cherry shrimp Neocaridina davidi (Caridea, Atyidae).Journal of the World Aquaculture Society, 51(3): 775-787. https://doi.org/10.1111/jwas.12660
https://doi.org/10.1111/jwas.12660...
).

Data analyses

The number of animals presenting each behavior was converted to frequency within the tank. The Wilcoxson test was used to compare shelter use frequency (regardless of type) between daytime and nighttime. The same test was used to analyze the frequency of moving individuals between daytime and nighttime. To assess the difference between shelter type usage and to compare the frequency of moving individuals during observation times we used the Friedman test, followed by the Student-Newman-Keuls test. A significance interval of 95% was used for all tests (Zar, 1999Zar JH 1999. Biostatistical Analysis. Prentice Hall. 663p.) for both general and group-related (male, non-ovigerous female, ovigerous female) results.

RESULTS

Shelter use

Neocaridina davidi presented highly cryptic behavior. In all observations, most individuals were using the shelters, with an average of 82.1 ± 8.69% sheltered individuals. The frequency of individuals using shelters was significantly higher during the daytime (88.79 ± 5.54%) than at nighttime (75.44 ± 5.53%) (Wilcoxson, Z = -24.7, P< 0.001). Ovigerous females presented more pronounced cryptic behavior, with an average of 88.81% ± 11.32% of individuals sheltered per observation while the average was 78.27 ± 9.90% for non-ovigerous females and 74.71% ± 13.17% for males. All experimental groups sheltered more during the daytime, particularly ovigerous females (Wilcoxson, Z = -16, P< 0.001) (Tab. 1).

Table 1.
Percentage of individuals of Neocaridina davidi (Bouvier, 1904) using shelters (average ± standard deviation) during the daytime and nighttime.

In all experimental groups, 7 am was the interval with the highest percentage of sheltered individuals. The proportion of sheltered individuals fluctuated throughout the daytime. There was a significant reduction in shelter use during the nighttime (Wilcoxson, P < 0.01) (Tab. 1, Fig. 3).

Table 2.
Frequency (average ± standard deviation) of moving individuals (walking or swimming), generally and by experimental group, during the daytime and nighttime.

Figure 3.
Frequency of individuals of Neocaridina davidi (Bouvier, 1904) using shelters at each observation time. The line inside the box indicates the median, box indicates the first and third quartiles and the whiskers indicate the minimum and maximum variation. A, General; B, males; C, non-ovigerous females; D, ovigerous females. Different letters indicate significant difference (P < 0.05).

Shelter type preference

The most frequently used shelter was Java moss, with an average of 41.14 ± 16.27% of individuals. The least used shelter was rock fragment, with an average of 2.47 ± 1.60% of individuals per observation, and it was also the shelter least used by all experimental groups (Fig. 4). The shelter most frequently used by males and ovigerous females was Java moss, with 31.01 ± 24.44 and 57.02 ± 22.01% of individuals per observation, respectively. For non-ovigerous females, wood was the most frequently used shelter type (35.70 ± 17.73%) although there was no significant difference between the use of this shelter type and Java moss for this class (35.38 ± 21.52; Friedman test, P> 0.05).

Figure 4.
Frequency of individuals of Neocaridina davidi (Bouvier, 1904) using each shelter type. The line inside the box indicates the median, box indicates the first and third quartiles and whiskers indicate the minimum and maximum variation. A, General; B, males; C, non-ovigerous females; D, ovigerous females. Different letters indicate significant difference (P < 0.05).

Activity pattern

The average frequency of moving animals during each observation was 4.80 ± 4.53%. Of these, 3.19 ± 1.71 % were walking and 6.42 ± 5.72% were swimming. Males moved more frequently (6.72 ± 7.02%) than both non-ovigerous females (4.08 ± 5.68%) and ovigerous females (3.80 ± 5.82%). During the daytime, the general moving frequency was 2.13 ± 1.33%. The majority of moving individuals were walking (2.56 ± 1.55%) while the average swimming frequency was 1.69% ± 0.92%. Most moving was recorded at nighttime. During this period, the general moving frequency was 7.49 ± 5.01% and there was an increase in both walking (3.82 ± 1.66%) and swimming (11.15 ± 4.52%) frequency. Males moved more frequently than the other experimental groups in both periods (daytime and nighttime) and ovigerous females presented a higher distinction in movement between periods (Tab. 2).

There was a difference in walking individuals between observation times (Friedman test, P< 0.05). Walking frequency was significantly lower at 7 am generally and for each class separately (Friedman test, P< 0.05). The remaining observation times varied slightly in walking frequency. The highest frequency values were recorded between 4 pm and 1 am. There is a clear separation of swimming individuals between periods. No significant difference was recorded during the daytime (7 am, 10 am, 1 pm, and 4 pm; Friedman test, P> 0.05), followed by a gradual increase of frequency during the nighttime, peaking at 4 am (Fig. 5).

Figure 5.
Frequency of individuals of Neocaridina davidi (Bouvier, 1904) swimming (left) and walking (right). A and B, General; C and D, males; E and F, non-ovigerous females; G and H, ovigerous females. Different letters indicate significant difference (P < 0.05).

DISCUSSION

We observed a highly cryptic behavior for N. davidi with a tendency of sheltering, especially during the daytime, confirming our initial hypothesis. As this species is frequently used in aquariums, providing shelter sites seems an essential measure to improve the wellness of individuals. By sheltering, individuals can overcome the potential stress of excessive light in open spaces.

The analyzed shrimps were inactive in most observation times with most of these individuals in shelters. However, there was variation regarding sex and reproductive status in females. Several factors can influence the use of shelters, such as shelter quality, individual social position, and the presence of other individuals in the same tank. These factors have also been observed for the freshwater prawn Macrobrachium australiense Holthuis, 1950 (Lammers et al., 2009Lammers JH, Warburton K and Bronwen WC 2009. Diurnal refuge competition in the freshwater prawn, Macrobrachium australiense. Journal of Crustacean Biology, 29(4): 476-483. https://doi.org/10.1651/08-3093.1
https://doi.org/10.1651/08-3093.1...
). The more pronounced cryptic behavior of ovigerous females can be related to the protection of the offspring, which is a natural strategy to ensure reproductive success, minimizing the number of eggs that could be lost or aborted due to exposure to predators and locomotion (Maciá and Robinson, 2009Maciá S and Robinson MP 2009. Why be cryptic? Choice of host urchin is not based on camouflage in the caridean shrimp Gnathophylloides mineri. Acta Ethologica, 12(2): 105-113. https://doi.org/10.1007/s10211-009-0064-7
https://doi.org/10.1007/s10211-009-0064-...
; Duarte and Flores, 2017Duarte RC and Flores AA 2017. Morph-specific habitat and sex distribution in the caridean shrimp Hippolyte obliquimanus. Journal of the Marine Biological Association of the United Kingdom, 97(2): 235-242. http://doi.org/10.1017/S0025315416000230
http://doi.org/10.1017/S0025315416000230...
; Pescinelli et al., 2017Pescinelli RA, Davanso TM and Costa RC 2017. Social monogamy and egg production in the snapping shrimp Alpheus brasileiro (Caridea: Alpheidae) from the south-eastern coast of Brazil. Journal of the Marine Biological Association of the United Kingdom, 97(7): 1519-1526. https://doi.org/10.1017/S0025315416000904
https://doi.org/10.1017/S002531541600090...
).

As for the activity behavior, we noticed that males are more active in comparison to females and ovigerous females, therefore, these individuals move more frequently in the tanks, even during daytime, but mainly at nighttime. This may be a natural reflection of the mating system called "pure search" (Sganga et al., 2016Sganga DE, Piana LR and Greco LS 2016. Sexual dimorphism in a freshwater atyid shrimp (Decapoda: Caridea) with direct development: a geometric morphometrics approach. Zootaxa, 4196(1): https://doi.org/10.11646/zootaxa.4196.1.7
https://doi.org/10.11646/zootaxa.4196.1....
; Vazquez et al., 2017Vazquez ND, Delevati-Colpo K, Sganga DE and López-Greco LS 2017. Density and gender segregation effects in the culture of the caridean ornamental red cherry shrimp Neocaridina davidi Bouvier, 1904 (Caridea: Atyidae). Journal of Crustacean Biology, 37(4): 367-373. https://doi.org/10.1093/jcbiol/rux051
https://doi.org/10.1093/jcbiol/rux051...
). In this system, males have a strategy to keep swimming in search of receptive females, when finding these females, these individuals copulate quickly and then the males go back to looking for other receptive females (Correa and Thiel, 2003Correa C and Thiel M 2003. Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Revista Chilena de História Natural, 76: 187-203. https://doi.org/10.4067/S0716-078X2003000200006
https://doi.org/10.4067/S0716-078X200300...
; Bauer, 2004Bauer RT 2004. Remarkable shrimps: adaptations and natural history of the carideans. Norman, University of Oklahoma Press. 316 p.). Therefore, the activity pattern observed in this study may be a reflection of the natural behavior and associated with the type of sexual system for this species, with males moving more frequently due to the search for sexual partners.

Although it has been recently demonstrated that the Java moss Vesicularia sp. in tanks does not affect N. davidi survivorship (Tomas et al., 2020Tomas AL, Sganga DE and Lopez Greco LS 2020. Effect of background color and shelters on female pigmentation in the ornamental red cherry shrimp Neocaridina davidi (Caridea, Atyidae).Journal of the World Aquaculture Society, 51(3): 775-787. https://doi.org/10.1111/jwas.12660
https://doi.org/10.1111/jwas.12660...
), this shelter type was the most frequently used by individuals. This higher frequency of use is probably related to its higher structural complexity, as it creates a three dimensional environment. Habitat complexity can determine organism distribution (Figueiredo et al., 2013Figueiredo BRS, Mormul RP and Benedito E 2013. Nonadditive effects of macrophyte cover and turbidity on predator-prey interactions involving an invertivorous fish and different prey types.Hydrobiologia, 716(1): 21-28. https://doi.org/10.1007/s10750-013-1540-7
https://doi.org/10.1007/s10750-013-1540-...
; Gartner et al., 2013Gartner A, Tuya F, Lavery PS and McMahon K 2013. Habitat preferences of macroinvertebrate fauna among seagrasses with varying structural forms.Journal of Experimental Marine Biology and Ecology, 439: 143-151. https://doi.org/10.1016/j.jembe.2012.11.009
https://doi.org/10.1016/j.jembe.2012.11....
). High complexity habitats present higher food availability due to a larger surface for microalgae colonization and provide greater protection against predators (Chemello and Milazzo, 2002Chemello R and Milazzo M 2002. Effect of algal architecture on associated fauna: some evidence from phytal molluscs.Marine Biology, 140(5): 981-990. https://doi.org/10.1007/s00227-002-0777-x
https://doi.org/10.1007/s00227-002-0777-...
). In an experiment with artificial shelters, Park et al. (2015Park KY, Park HG and Kwon ON 2015. Effects of stocking density and shelter type on the growth and survival of pandalid shrimp (Pandalopsis japonica Balss, 1914) juveniles.Crustaceana, 88(2): 144-151. https://doi.org/10.1163/15685403-00003407
https://doi.org/10.1163/15685403-0000340...
) observed a higher number of juvenile Pandalopsis japonica Balls, 1914 attached to the brush-type shelter and related this finding to the higher availability of independent spaces in relation to the other shelter types.

The only sex class in which Java moss was not the most frequently used shelter type was non-ovigerous females. Similar to Macrobrachium brasiliense (Heller, 1862) (Nogueira et al., 2018Nogueira CS, Costa TM and Almeida AC 2018. Habitat choice behavior in Macrobrachium brasiliense (Heller, 1862) (Decapoda, Palaemonidae) under laboratory conditions.Oecologia Australis, 22(1): 55-62. https://doi.org/10.4257/oeco.2018.2201.05
https://doi.org/10.4257/oeco.2018.2201.0...
), this sex class used the wood shelters more frequently. According to the authors, wood favors biofilm formation while presenting gaps that can be used as hiding sites. The wood itself is a decaying matter source, which would favor biofilm formation on its own. Rock was the least used shelter type by all experimental groups, probably due to its three dimensional characteristics and lower structural complexity.

We observed a circadian rhythm regarding moving activity of N. davidi. Moving activity peaked at dawn, decreasing abruptly throughout the day. There was an increase in moving activity at 10 am and another decrease in frequency at the beginning of the afternoon. Several marine and freshwater caridean shrimps present higher activity during the night (Guerao, 1995Guerao G 1995. Locomotor activity patterns and feeding habits in the prawn Palaemonxiphias (Crustacea: Decapoda: Palaemonidae) in Alfacs Bay, Ebro Delta (northwest Mediterranean). Marine Biology, 122: 115-119. https://doi.org/10.1007/BF00349284
https://doi.org/10.1007/BF00349284...
; Guerao and Ribeira, 1996Guerao G and Ribera C 1996. Locomotor activity patterns and feeding habits in the prawnPalaemon serratus(Pennant, 1777) (Decapoda, Palaemonidae) in the Alfa Bay, Elbro Delta, Spain.Crustaceana, 69(1): 101-112. ). This pattern has also been reported for Dendrobranchiata and other decapod groups, especially as a strategy of protection against visual predators, such as fish (Dall et al., 1990; Pontes, 2006; Ogburn et al., 2013Ogburn MB, Criales MM, Thompson RT and Browder JA 2013. Endogenous swimming activity rhythms of postlarvae and juveniles of the penaeid shrimp Farfantepenaeus aztecus, Farfantepenaeus duorarum, and Litopenaeus setiferus.Journal of Experimental Marine Biology and Ecology, 440: 149-155. https://doi.org/10.1016/j.jembe.2012.12.007
https://doi.org/10.1016/j.jembe.2012.12....
; Trevisan et al., 2015Trevisan A, Marochi MZ and Masunari S 2014. Circadian rhythm in males of Aegla schmitti (Decapoda, Anomura, Aeglidae) under laboratory conditions.Biological Rhythm Research, 45(5): 80-816. https://doi.org/10.1080/09291016.2014.921410
https://doi.org/10.1080/09291016.2014.92...
). Furthermore, there was an increase in the swimming frequency of all experimental groups at nighttime. Such an increase was also observed in juveniles of Macrobrachium rosenbergii (de Man, 1879) (Scudder et al., 1981Scudder K, Pasanello E, Krafsur J and Ross K 1981. Analysis of locomotory activity in juvenile giant Malaysian prawns, Macrobrachium rosenbergii (De Man) (Decapoda, Palaemonidae). Crustaceana, 40(1): 31-35. ) and in females of Palaemon varians Leach, 1814 and P. longirostris H. Milne Edwards, 1837 (Finchan and Furlong, 1984Fincham AA and Furlong JA 1984. Seasonal swimming rhythms of female palaemonid estuarine prawns and shrimps.Journal of Natural History, 18(3): 425-439. https://doi.org/10.1080/00222938400770361
https://doi.org/10.1080/0022293840077036...
).

We observed a cryptic behavior for N. davidi with a tendency of sheltering during the daytime, especially for females and even more for ovigerous ones. Java moss (Vesicularia sp.) was the most used shelter type and therefore recommended for microhabitat composition in tanks for aquarists. Finally, we have here demonstrated an increase in activity during nighttime and a shift in moving patterns between periods. While walking was predominant during the daytime, swimming was more frequent during the nighttime. This might be a reflection of natural behavior corresponding to the period of searching for food and sexual partners.

ACKNOWLEDGEMENTS

We are grateful to all our laboratory colleagues and coworkers for their help during the experimental procedures.

REFERENCES

  • Aguzzi J, Abelló P and García JA 2006. Daily activity patterns of the mud shrimp Solenocera membranacea (Decapoda: Penaeoidea: Solenoceridae) in the western Mediterranean: a Comparison by Depth and Season.Bulletin of Marine Science, 79(2): 353-364.
  • Bauer RT 2004. Remarkable shrimps: adaptations and natural history of the carideans. Norman, University of Oklahoma Press. 316 p.
  • Cai Y 1996. A revision of the genus Neocaridina (Crustacea, Decapoda, Atyidae). Acta Zootaxonomica Sinica, 21(2): 129-160.
  • Calado R, Dionísio G, Bartilotti C, Nunes C, Santos A and Dinis MT 2008. Importance of light and larval morphology in starvation resistance and feeding ability of newly hatched marine ornamental shrimpsLysmataspp. (Decapoda: Hippolytidae). Aquaculture, 283(1-4): 56-63. https://doi.org/10.1016/j.aquaculture.2008.07.010
    » https://doi.org/10.1016/j.aquaculture.2008.07.010
  • Carvalho-Batista A, Castilho AL, Fransozo A and Costa RC 2012. Diel comparison of the catch and size of the shrimp Artemesia longinaris (Dendrobranchiata, Penaeidae) in the Ubatuba region, northern coast of the state of São Paulo.Crustaceana, 85(10): 1179-1191. https://doi.org/10.1163/15685403-00003122
    » https://doi.org/10.1163/15685403-00003122
  • Chemello R and Milazzo M 2002. Effect of algal architecture on associated fauna: some evidence from phytal molluscs.Marine Biology, 140(5): 981-990. https://doi.org/10.1007/s00227-002-0777-x
    » https://doi.org/10.1007/s00227-002-0777-x
  • Correa C and Thiel M 2003. Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Revista Chilena de História Natural, 76: 187-203. https://doi.org/10.4067/S0716-078X2003000200006
    » https://doi.org/10.4067/S0716-078X2003000200006
  • Duarte RC and Flores AA 2017. Morph-specific habitat and sex distribution in the caridean shrimp Hippolyte obliquimanus Journal of the Marine Biological Association of the United Kingdom, 97(2): 235-242. http://doi.org/10.1017/S0025315416000230
    » http://doi.org/10.1017/S0025315416000230
  • Edwards DH and Herberholz J 2005. Crustacean models of aggression, p. 38-61. In: RJ Nelson (Ed.), Biology of aggression. Oxford, UK, Oxford University Press. 528p.
  • Elwood RW, Barr S and Patterson L 2009. Pain and stress in crustaceans? Applied Animal Behaviour Science, 118(3-4): 128-136. https://doi.org/10.1016/j.applanim.2009.02.018
    » https://doi.org/10.1016/j.applanim.2009.02.018
  • Elwood RW 2012. Evidence for pain in decapod crustaceans. Animal Welfare, 21(1): 23-27. https://doi.org/10.7120/096272812X13353700593365
    » https://doi.org/10.7120/096272812X13353700593365
  • Fanjul-Moles ML, Bosques-Tistler T, Prieto-Sagredo J, Castanón-Cervantes O and Fernández-Rivera-Rıo L 1998. Effect of variation in photoperiod and light intensity on oxygen consumption, lactate concentration and behavior in crayfish Procambarus clarkii and Procambarus diguetiComparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 119(1), 263-269. https://doi.org/10.1016/S1095-6433(97)00413-3
    » https://doi.org/10.1016/S1095-6433(97)00413-3
  • Farhadi A and Jensen MA 2016. Effects of photoperiod and stocking density on survival, growth and physiological responses of narrow clawed crayfish (Astacus leptodactylus).Aquaculture Research, 47(8): 2518-2527. https://doi.org/10.1111/are.12700
    » https://doi.org/10.1111/are.12700
  • Fincham AA and Furlong JA 1984. Seasonal swimming rhythms of female palaemonid estuarine prawns and shrimps.Journal of Natural History, 18(3): 425-439. https://doi.org/10.1080/00222938400770361
    » https://doi.org/10.1080/00222938400770361
  • Figueiredo BRS, Mormul RP and Benedito E 2013. Nonadditive effects of macrophyte cover and turbidity on predator-prey interactions involving an invertivorous fish and different prey types.Hydrobiologia, 716(1): 21-28. https://doi.org/10.1007/s10750-013-1540-7
    » https://doi.org/10.1007/s10750-013-1540-7
  • Fischer JR, Gangloff MM and Creed RP 2020. The behavioral responses of 2 appalachian crayfish to cool and warm spectrum led lights at night.Freshwater Science, 39(1), 39-46. https://doi.org /10.1086/707459
    » https://doi.org /10.1086/707459
  • Fossat P, Bacqué-Cazenave J, De Deurwaerdère P, Delbecque JP and Cattaert D 2014. Anxiety-like behavior in crayfish is controlled by serotonin.Science, 344(6189): 1293-1297. https://doi.org/10.1126/science.1248811
    » https://doi.org/10.1126/science.1248811
  • Gartner A, Tuya F, Lavery PS and McMahon K 2013. Habitat preferences of macroinvertebrate fauna among seagrasses with varying structural forms.Journal of Experimental Marine Biology and Ecology, 439: 143-151. https://doi.org/10.1016/j.jembe.2012.11.009
    » https://doi.org/10.1016/j.jembe.2012.11.009
  • Granado P, De Grande FR and Costa TM. 2020. Association of Epialtus brasiliensis Dana, 1852 (Brachyura, Majoidea) with different species of seaweed.Nauplius, 28: e2020004. https://doi.org/10.1590/2358-2936e2020004
    » https://doi.org/10.1590/2358-2936e2020004
  • Guerao G 1995. Locomotor activity patterns and feeding habits in the prawn Palaemonxiphias (Crustacea: Decapoda: Palaemonidae) in Alfacs Bay, Ebro Delta (northwest Mediterranean). Marine Biology, 122: 115-119. https://doi.org/10.1007/BF00349284
    » https://doi.org/10.1007/BF00349284
  • Guerao G and Abelló P 1996. Patterns of activity in the sympatric prawns Palaemon adspersus and Processa edulis (Decapoda, Caridea) from a shallow Mediterranean bay. Scientia Marina, 60(2-3): 319-324.
  • Guerao G and Ribera C 1996. Locomotor activity patterns and feeding habits in the prawnPalaemon serratus(Pennant, 1777) (Decapoda, Palaemonidae) in the Alfa Bay, Elbro Delta, Spain.Crustaceana, 69(1): 101-112.
  • Hindley JPR 1975. Effects of endogenous and some exogenous factors on the activity of juvenile banana prawnPenaeus merguiensisMarine Biology, 29: 1-8. https://doi.org/10.1007/BF00395521
    » https://doi.org/10.1007/BF00395521
  • Jablonska A, Mamos T, Gruska P, Szlauer-Lukaszewska A and Grabowski M 2018. First record and DNA barcodes of the aquarium shrimp, Neocaridina davidi, in Central Europe from thermally polluted River Oder canal, Poland. Knowledge and Management of Aquatic Ecosystems, 419(14): 1-5. https://doi.org/10.1051/kmae/2018004
    » https://doi.org/10.1051/kmae/2018004
  • Jones CM and Ruscoe IM 2001. Assessment of Five Shelter Types in the Production of Redclaw Crayfish Cherax quadricarinatus (Decapoda: Parastacidae) Under Earthen Pond Conditions. Journal of the World Aquaculture Society, 32(1): 41-52. https://doi.org/10.1111/j.1749-7345.2001.tb00920.x
    » https://doi.org/10.1111/j.1749-7345.2001.tb00920.x
  • Klotz W, Miesen FW, Hullen S and Herder F 2013. Two Asian freshwater shrimp species found in a thermally polluted stream system in North Rhine-Westphalia, Germany. Aquatic Invasions, 8(3): 333-339. http://dx.doi.org/10.3391/ai.2013.8.3.09
    » http://dx.doi.org/10.3391/ai.2013.8.3.09
  • Lammers JH, Warburton K and Bronwen WC 2009. Diurnal refuge competition in the freshwater prawn, Macrobrachium australiense Journal of Crustacean Biology, 29(4): 476-483. https://doi.org/10.1651/08-3093.1
    » https://doi.org/10.1651/08-3093.1
  • Liang XQ 2004. Fauna Sinica. Invertebrata: Crustacea: Decapoda: Atyidae Science Press, Beijing, China, 375p.
  • Lorenzi H 2008. Plantas daninhas do Brasil: terrestres, aquáticas, parasitas e tóxicas. 4ª ed., Nova Odessa, Instituto Plantarum, 640p.
  • Maciá S and Robinson MP 2009. Why be cryptic? Choice of host urchin is not based on camouflage in the caridean shrimp Gnathophylloides mineri Acta Ethologica, 12(2): 105-113. https://doi.org/10.1007/s10211-009-0064-7
    » https://doi.org/10.1007/s10211-009-0064-7
  • Magee B and Elwood RW 2013. Shock avoidance by discrimination learning in the shore crab (Carcinus maenas) is consistent with a key criterion for pain. Journal of Experimental Biology, 216(3): 353-358. https://doi.org/10.1242/jeb.072041
    » https://doi.org/10.1242/jeb.072041
  • Marshall S, Warburton K, Paterson B and Mann D 2005. Cannibalism in juvenile blue-swimmer crabs Portunus pelagicus (Linnaeus, 1766): effects of body size, moult stage and refuge availability. Applied Animal Behaviour Science, 90(1): 65-82. https://doi.org/10.1016/j.applanim.2004.07.007
    » https://doi.org/10.1016/j.applanim.2004.07.007
  • Martin P, Bateson PPG and Bateson P 1993. Measuring behaviour: an introductory guide. Cambridge, Cambridge University Press. 246p.
  • Mitsugi M and Suzuki H 2018. Life history of an invasive freshwater shrimp Neocaridina davidi (Bouvier, 1904), (Decapoda: Caridea: Atyidae) in the Tomoe River, the Boso Peninsula, eastern Japan. Crustacean Research, 47: 9-16. https://doi.org/10.18353/crustacea.47.0_9
    » https://doi.org/10.18353/crustacea.47.0_9
  • Moller TH and Jones DA 1975. Locomotory rhythms and burrowing habits of Penaeus semisulcatus (de Haan) and P. monodon (Fabricius) (Crustacea: Penaeidae).Journal of Experimental Marine Biology and Ecology, 18(1): 61-77. https://doi.org/10.1016/0022-0981(75)90017-9
    » https://doi.org/10.1016/0022-0981(75)90017-9
  • Negrisoli E, Martins D, Velini DE and Ferrera WLB 2003. Degradação de diquat em condições de caixa d'água com e sem plantas de egéria.Planta Daninha, 21: 93-98. https://doi.org/10.1590/S0100-83582003000400014
    » https://doi.org/10.1590/S0100-83582003000400014
  • Nogueira CS, Costa TM and Almeida AC 2018. Habitat choice behavior in Macrobrachium brasiliense (Heller, 1862) (Decapoda, Palaemonidae) under laboratory conditions.Oecologia Australis, 22(1): 55-62. https://doi.org/10.4257/oeco.2018.2201.05
    » https://doi.org/10.4257/oeco.2018.2201.05
  • Ogburn MB, Criales MM, Thompson RT and Browder JA 2013. Endogenous swimming activity rhythms of postlarvae and juveniles of the penaeid shrimp Farfantepenaeus aztecus, Farfantepenaeus duorarum, and Litopenaeus setiferusJournal of Experimental Marine Biology and Ecology, 440: 149-155. https://doi.org/10.1016/j.jembe.2012.12.007
    » https://doi.org/10.1016/j.jembe.2012.12.007
  • Pantaleão JAF, Barros-Alves SP, Tropea C, Alves DFR, Negreiros-Fransozo ML and López-Greco LS 2015. Nutritional vulnerability in early stages of the freshwater ornamental red cherry shrimp. Neocaridina davidi (Bouvier, 1904) (Caridea: Atyidae). Journal of Crustacean Biology, 35(5): 676-681. https://doi.org/10.1163/1937240X-00002357
    » https://doi.org/10.1163/1937240X-00002357
  • Pantaleão JAF, Gregati RA, Costa RC, López‐Greco LS and Negreiros‐Fransozo ML 2017. Post‐hatching development of the ornamental ‘Red Cherry Shrimp’ Neocaridina davidi (Bouvier, 1904) (Crustacea, Caridea, Atyidae) under laboratorial conditions. Aquaculture Research, 48(2): 553-569. https://doi.org/10.1111/are.12903
    » https://doi.org/10.1111/are.12903
  • Park KY, Park HG and Kwon ON 2015. Effects of stocking density and shelter type on the growth and survival of pandalid shrimp (Pandalopsis japonica Balss, 1914) juveniles.Crustaceana, 88(2): 144-151. https://doi.org/10.1163/15685403-00003407
    » https://doi.org/10.1163/15685403-00003407
  • Pescinelli RA, Davanso TM and Costa RC 2017. Social monogamy and egg production in the snapping shrimp Alpheus brasileiro (Caridea: Alpheidae) from the south-eastern coast of Brazil. Journal of the Marine Biological Association of the United Kingdom, 97(7): 1519-1526. https://doi.org/10.1017/S0025315416000904
    » https://doi.org/10.1017/S0025315416000904
  • Rodriguez G and Naylor E 1972. Behavioural rhythms in littoral prawns.Journal of Marine Biology Association, 52(1): 81-95. https://doi.org/10.1017/S0025315400018592
    » https://doi.org/10.1017/S0025315400018592
  • Santos ADA, López-Olmeda JF, Sánchez-Vázquez FJ and Fortes-Silva R 2016. Synchronization to light and mealtime of the circadian rhythms of self-feeding behavior and locomotor activity of white shrimps (Litopenaeus vannamei).Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 199: 54-61. https://doi.org/10.1016/j.cbpa.2016.05.001
    » https://doi.org/10.1016/j.cbpa.2016.05.001
  • Schneider CA, Rasband WS and Eliceiri KW 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9: 671-675. https://doi.org/10.1038/nmeth.2089
    » https://doi.org/10.1038/nmeth.2089
  • Schoolmann G and Arndt H 2018. Population dynamics of the invasive freshwater shrimp Neocaridina davidi in the thermally polluted Gillbach stream (North Rhine-Westphalia, Germany). Limnologica, 71: 1-7. https://doi.org/10.1016/j.limno.2018.05.001
    » https://doi.org/10.1016/j.limno.2018.05.001
  • Scudder K, Pasanello E, Krafsur J and Ross K 1981. Analysis of locomotory activity in juvenile giant Malaysian prawns, Macrobrachium rosenbergii (De Man) (Decapoda, Palaemonidae). Crustaceana, 40(1): 31-35.
  • Sganga DE, Piana LR and Greco LS 2016. Sexual dimorphism in a freshwater atyid shrimp (Decapoda: Caridea) with direct development: a geometric morphometrics approach. Zootaxa, 4196(1): https://doi.org/10.11646/zootaxa.4196.1.7
    » https://doi.org/10.11646/zootaxa.4196.1.7
  • Smith MJ and Williams WD 1980. Infraspecific variations within the Atyidae: a study of morphological variation within a population of Paratya australiensis (Crustacea: Decapoda). Marine and Freshwater Research, 31(3): 397-407. https://doi.org/10.1071/MF9800397
    » https://doi.org/10.1071/MF9800397
  • Tomas AL, Sganga DE and Lopez Greco LS 2020. Effect of background color and shelters on female pigmentation in the ornamental red cherry shrimp Neocaridina davidi (Caridea, Atyidae).Journal of the World Aquaculture Society, 51(3): 775-787. https://doi.org/10.1111/jwas.12660
    » https://doi.org/10.1111/jwas.12660
  • Trevisan A, Marochi MZ and Masunari S 2014. Circadian rhythm in males of Aegla schmitti (Decapoda, Anomura, Aeglidae) under laboratory conditions.Biological Rhythm Research, 45(5): 80-816. https://doi.org/10.1080/09291016.2014.921410
    » https://doi.org/10.1080/09291016.2014.921410
  • Vazquez ND, Delevati-Colpo K, Sganga DE and López-Greco LS 2017. Density and gender segregation effects in the culture of the caridean ornamental red cherry shrimp Neocaridina davidi Bouvier, 1904 (Caridea: Atyidae). Journal of Crustacean Biology, 37(4): 367-373. https://doi.org/10.1093/jcbiol/rux051
    » https://doi.org/10.1093/jcbiol/rux051
  • Włodarczyk A, Sonakowska L, Kamińska K, Marchewka A, Wilczek G, Wilczek P, Student S and Rost-Roszkowska M 2017. The effect of starvation and re-feeding on mitochondrial potential in the midgut ofNeocaridina davidi(Crustacea, Malacostraca). PLoS ONE, 12(3): e0173563. https://doi.org/10.1371/journal.pone.0173563
    » https://doi.org/10.1371/journal.pone.0173563
  • Włodarczyk A, Wilczek G, Wilczek P, Student S, Ostróżka A, Tarnawska M and Rost-Roszkowska M 2019. Relationship between ROS production, MnSOD activation and periods of fasting and re-feeding in freshwater shrimpNeocaridina davidi(Crustacea, Malacostraca).PeerJ, 7: e7399. https://doi.org/10.7717/peerj.7399
    » https://doi.org/10.7717/peerj.7399
  • Wowor D, Cai Y and Ng PKL 2004. Crustacean: Decapoda: Caridea, p. 337-357. In: C Yule and HS Yong (eds), The Freshwater Invertebrates of Malaysia and Singapore. Malaysian Academy of Sciences.
  • Zar JH 1999. Biostatistical Analysis. Prentice Hall. 663p.

ADDITIONAL INFORMATION AND DECLARATIONS

  • Author Contributions

    AC-B, CSN, and JAFP equally contributed to the design, execution, and analysis of the experimental results. All authors equally contributed to the writing and revision of the manuscript.
  • Consent for publication

    All authors declare that they have reviewed the content of the manuscript and gave their consent to submit the document.
  • Data availability

    The data that support the findings of this study are available from the corresponding author, AC-B, upon reasonable request
  • Funding and grant disclosures

    RCC thank the National Council for Scientific and Technological Development - CNPq (Research Scholarships PQ # 304368/2022-9) and São Paulo Research Foundation - FAPESP (Biota INTERCRUSTA 2018/13685-5).
  • Study association

    This study was conducted at the Laboratório de Biologia de Camarões (LABCAM) and is part of the research focus of the group.
  • Study permits

    This study was conducted under the permission (SISBIO n° 23012-3) issued by the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA).

Edited by

Associate Editor:

Antonio Castilho

Editor-in-chief:

Christopher Tudge

Data availability

The data that support the findings of this study are available from the corresponding author, AC-B, upon reasonable request

Publication Dates

  • Publication in this collection
    22 Sept 2023
  • Date of issue
    2023

History

  • Received
    24 Oct 2021
  • Accepted
    13 Oct 2022
Sociedade Brasileira de Carcinologia Instituto de Biociências, UNESP, Campus Botucatu, Rua Professor Doutor Antônio Celso Wagner Zanin, 250 , Botucatu, SP, 18618-689 - Botucatu - SP - Brazil
E-mail: editor.nauplius@gmail.com