The effect of spirulina (Arthrospira platensis) (Oscillatoriales: Cyanobacteria) on the experimental breeding of Pseudosuccinea columella (Basommatophora: Lymnaeidae)
Efecto de la espirulina (Arthrospira platensis) (Oscillatoriales: Cyanobacteria) en la cría experimental de Pseudosuccinea columella (Basommatophora: Lymnaeidae)
Lucila Prepelitchi1*, Julieta M. Pujadas1 & Cristina Wisnivesky-Colli1
Abstract ]]>
Snails of the family Lymnaeidae, as Pseudosuccinea columella, are the intermediate hosts of Fasciola hepatica, the causative agent of fasciolosis in human and livestock all over the world. A thorough knowledge of snail biology is essential for describing the transmission dynamics and for controlling this disease. Since food quality has had a significant effect on snail growth, ]]>
Arthrospira platensis) as a food resource for the artificial breeding of P. columella, an invasive snail and the main intermediate host of F. hepatica in Northeastern Argentina. The main purpose was to measure the effect of spirulina on fitness parameters such as survival rate, growth rate, size at first reproduction, lifetime fecundity and viable offspring. A total of 20 676 newly-laid F2 eggs were ]]>
P. columella snails fed only with lettuce, we found that P. columella fed with ]]>
P. columella diet with ]]>
P. columella development by consuming it, along with an indirect positive effect by improving the water quality. This rearing technique provided large number of reproducing adults and a continuous production of offspring, which are essential for developing future experimental studies in order to improve our knowledge on P. columella biology.
Los caracoles de la familia Lymneidae, ]]>
Pseudosuccinea columella, actúan como hospedadores intermediarios de Fasciola hepatica, el agente etiológico de la fasciolosis, zoonosis que afecta al ganado y al hombre en todo el mundo. Conocer profundamente las características biológicas de estos caracoles resulta ]]>
Arthrospira platensis) como fuente de alimento para la cría artificial de P. ]]>
, una especie invasora que actúa como el principal hospedero intermediario de F. hepatica en el Noreste Argentino. El objetivo principal de este trabajo fue medir el efecto de la espirulina en parámetros del fitness tales como: tasa de supervivencia, tasa de crecimiento, tamaño que alcanzan a la madurez sexual, duración del período ]]>
F2 recién puestos; la mitad de ellos fue alimentado con lechuga (tratamiento L) y la otra mitad con lechuga mas espirulina (tratamiento L+S). En comparación con las P. columella alimentadas solamente ]]>
P. columella alimentadas con lechuga mas espirulina: 1) presentaron mayores tasas de supervivencia, 2) alcanzaron mayores tamaños y en menor tiempo, 3) alcanzaron la madurez sexual antes de tiempo (L+S:60 días vs. L:120 días) y a menor tamaño (L+S:4.8mm vs. L:8.2mm), 4) tuvieron un período reproductivo más largo (L+S:150 días vs. L:90 días), 5) produjeron mayor cantidad de ]]>
P. columella y maximizó la cría artificial de esta especie en laboratorio. La espirulina podría tener un efecto positivo directo sobre el desarrollo de P. columella mediante su consumo, pero también podría tener un efecto positivo indirecto al mejorar la calidad del agua. Con la técnica de cría desarrollada en este trabajo se obtiene una gran cantidad de caracoles adultos reproductores y una continua producción de huevos que son esenciales para desarrollar futuros estudios que permitan aumentar nuestro conocimiento sobre la biología de P. columella.
Snails of the family Lymnaeidae act as intermediate hosts of several trematodes of medical and veterinary importance. Among these is Fasciola ]]>
(Linnaeus, 1758), the causative agent of fasciolosis in human and livestock all over the world (Malek, 1985). This zoonotic disease causes great economic losses due to liver condemnation, increased mortality and decreased milk, wool and meat production (Hope-Cawdery, Strickland, Conway, & Crowe, 1977; Boray, 1981). To be effective, control measures should be based on a sound understanding of the epidemiology of fasciolosis, which depends mainly on environmental factors that affects the free-living stages of F. hepatica and the intermediate host populations of lymnaeid snails (Torgerson, & Claxton, 1999). In addition, F. hepatica presents high specificity and compatibility towards its intermediate hosts (Cañete, Yong, Sánchez, Wong, & ]]>
In nature, snails thrive under diverse and changing environmental conditions, making it highly difficult to calculate essential biological variables such as growth rate, fecundity, survival and longevity (Eveland, & Haseeb, 2011). These biological characteristics are often studied under ]]>
Arthrospira platensis (Nordstedt) Gomont is the scientific name ]]>
To date, no ]]>
Lymnaea stagnalis (Linnaeus, 1758) and Lymnaea natalensis (Krauss, 1848) (DeKock, & Joubert, 1989; Khan, & Spencer, 2009). ]]>
Pseudosuccinea columella (Say, 1817) is a North American species (Malek, 1985) with a great potential to invade new areas (Boray, Fraser, Williams, & Wilson, 1984; DeKock, Joubert, & Petrorius, 1989). Actually it has a worldwide distribution and was reported in Europe, Oceania, Africa and America (Madsen, & Frandsen, 1989). In Central and South America,
P. columella enlarged its distribution area and was reported from Cuba (Gutiérrez, Pointier, Yong, Sanchez, & Theron, 2003), Guadalupe island (Durand et al., 2002), Puerto Rico, Mexico, Jamaica, Guatemala, Costa Rica, Panamá, Ecuador, Brasil, Paraguay, Argentina (Paraense, 1982), Colombia (Salazar, Estrada, & Velásquez, 2006), Venezuela (Malek, & Chrosciechowski, 1964), Uruguay (Heinzen, Castro, Pepe, & Ibarburu, 1994) and Perú (Larrea, Flórez, Vivar, Huamán, & ]]>
P. columella as intermediate host of F. hepatica was confirmed in Cuba (Gutiérrez et al., 2011), Colombia (Salazar et al., 2006), Brazil (Coelho, Lima, & Guimaraes, 2009), Argentina (Prepelitchi et al., 2003), New Zealand (Harris, & ]]>
Most of the knowledge about this non-native species comes from ecological works developed in the field (Prepelitchi et al., 2011). No experimental studies have been performed to study the biology of this species, and this information would be useful to better understand the ecological results as well as the role ]]>
P. columella in the transmission of F. hepatica.
The objective of this work was to ]]>
P. columella. The major purpose is to measure the effect of spirulina on fitness parameters such as survival, growth, size at first reproduction, lifetime fecundity and viable offspring of P. columella
. The ultimate goal is to develop a breeding system that provides a large number of reproducing adults and a continuous production of offspring to be used in future biological assays, in order to increase our knowledge on this invasive and biomedically important species.
Materials and Methods
Wild Pseudosuccinea columella snails were collected in the locality of Berón de Astrada (27°33’13’’ S - 57°32’51’’ W), Corrientes province, Northeastern Argentina and transported alive to the laboratory. Wild and first-generation (F1) P. columella snails were raised in 1.5L glass aquaria filled with 1L of dechlorinated and aerated filtered water. Water temperature was maintained at 22.5ºC±1.5 and snails were kept under a 12:12 light:dark photoperiod and fed ad libitum with lettuce leaves (Lactuca sativa).
]]>
A total of 20 676 newly-laid F2 eggs were used to test the effect of spirulina (Arthrospira platensis) on P. columella fitness parameters. Half of the eggs were fed with lettuce leaves (treatment L) and the other half with lettuce leaves plus spirulina (treatment L+S). Spirulina was purchased in a dry, powdered form (Algas de Tierra del Fuego®, Ushuaia, Tierra del Fuego, Argentina) and was dissolved in dechlorinated filtered water to obtain a stock solution of 33.3mg/mL.
Each treatment was ]]>
Snails in each glass aquarium were followed from laying to death (lifetime). Treatments ended when the last F2P. columella adult had died.
Every three days, all aquaria were cleaned, water was changed, unconsumed food and dead snails were discarded, and clean filtered water and fresh food were added as per the treatment protocol. ]]>
The number of F2 eggs that successfully hatched was counted and the date of hatching was registered in each of the six replicates of treatments L and L+S.
Following hatching, the number of ]]>
When the first F3 egg capsule was discovered in a glass aquarium, the shell length of all the live snails inside that recipient were measured to determine the mean size at first reproduction. The date was also recorded to determine the age at first reproduction. All newly-laid F3 eggs were removed from their parents aquarium and placed in newly glass aquaria, where they were monitored until they hatched. The number of F3
eggs that successfully hatched was registered.
Once a month, water temperature, pH, conductivity and dissolved oxygen were measured using a Sper Scientific® water quality meter (850081), and carbonate, general hardness, nitrite, amonia and carbon dioxide were measured with a Tetratest® Laborett Kit. ]]>
The experiment was a repeated measure design with repeated measures of snail growth and survival over time, with glass aquaria as the experimental units. Growth (defined by the dependent variable of mean shell length) and survival (defined by the dependent variable of number of live snails) were analyzed using the repeated measures generalized linear model (RM-GLM) procedure of Infostat V.12 software (Di-Rienzo et al., 2012). Treatments, days-post laying (time) and treatment by time interaction were included in the ]]>
Growth increment (G) was calculated using increments of mean shell length according to the following equation: G=(W1-W0)/(t1-t0) ]]>
0 and W1 are the mean shell length at times t0 and t1, respectively (Nasution, & Roberts, 2004).
F2 and F3 hatching rates, measured as proportions, were compared between treatments using a Chi-squared (χ2) test for independent samples (Fleiss, 1981). ]]>
Mean shell length at first egg-laying (sexual maturity) and lifetime fecundity (total F3 egg production) were recorded and compared between treatments using the nonparametric Mann-Whitney U-test for independent samples (Daniel, 1990).
]]>
Water chemistry measurements were compared between treatments using the nonparametric Mann-Whitney U-test for independent samples (Daniel, 1990).
In all cases, differences were considered significant at p<0.05. Statistical analyses were performed using the Infostat V.12 software (Di-Rienzo et al., 2012).
Results
The repeated measures generalized linear model on survival of Pseudosuccinea ]]>
snails demonstrated a significant treatment by time interaction (F8,85=4 144.39, p<0.0001; Fig. 1). Pseudosuccinea columellaF2 eggs began ]]>
Fig. 1). From hatching onwards, P. columella snails fed with spirulina showed significantly higher survival rates, in comparison with snails fed only with lettuce ]]>
P. columella snails fed with spirulina (Fig. 1). Maximum life-span of P. columella snails was 262 days.
The repeated measures generalized linear model on growth of Pseudosuccinea columella
snails revealed a significant interaction between treatment and time (F8,80 =4.67, p<0.0001; Fig. 2A). Between hatching (15 dpl) and 150 dpl, P. columella snails fed with spirulina (treatment L+S) were significantly bigger than snails fed only with lettuce (treatment L) (LSD, p<0.05 for treatment comparisons at each time interval). From 180 dpl onwards, ]]>
Fig. 2A). After 240 days, mean shell lengths (±SD) of snails fed with and without spirulina were 14.97±0.21 and 14.32±0.97mm, respectively.
Pseudosuccinea columella snails fed ]]>
Figure 2B. Snails fed with spirulina (treatment L+S) showed a low initial growth increment, followed by a high and sustained increase of this parameter between 60 and 150 dpl, after which growth increment gradually decrease (Fig. 2B). In contrast, snails fed only with lettuce (treatment L) showed a very low growth increment during their first month of life (30-60 dpl) and then ]]>
P. columella snails fed with spirulina. From 180 dpl onward, growth increment gradually decreases in both treatments (Fig. 2B).
The reproductive ]]>
P. columella also differed between treatments. P. columella snails fed with spirulina attained sexual maturity at a smallest size (mean shell length=4.8mm; n=1 907) in comparison to P. ]]>
fed only with lettuce (mean shell length=8.2mm, n=177; U=15.0, p<0.01). In addition, P. columella fed with spirulina reached sexual maturity at day 60 post-laying, whilst those fed without spirulina at day 120 post-laying. The duration of the reproductive period was of 150 days ]]>
P. columella fed with and without spirulina, respectively. Finally, the total number of eggs deposited per adult snail was also higher in treatment L+S (29.6 vs 13.3; U=4.0, p<0.04).
The number of eggs laid per adult P. columella fed with spirulina increased gradually between 60 and 120 dpl (1.6 and 34.6 eggs/adult, respectively), peaked at 180 dpl (56.7 eggs/adult) and decreased at 210 dpl (31.5 eggs/adult), which was the end of their reproductive period. In contrast, the maximum number of eggs laid per adult P. columella
fed only with lettuce was between 120 and 150 dpl (23.4 and 27.7 eggs/adult, respectively), and drastically decreased from 180 dpl onwards (4.2 eggs/adult). The viability of these eggs also differed between treatments. The percentage of viable F3 offspring in L+S was significantly higher (70% vs 40%; χ2=76.85, p<0.05).
Water chemistry ]]>
Table 1. The water from glass aquaria where snails were fed with lettuce plus spirulina showed higher values of conductivity, dissolved oxygen, carbonate, general hardness, nitrite and carbon dioxide, lower values of ammonia and equal values of pH and temperature (Table 1).
Discussion
Our results clearly showed the benefits of using spirulina as a dietary supplement for breeding P. columella under laboratory conditions. Individuals fed with lettuce ]]>
The hatching date (15 dpl) of the F2 eggs and their percentage of hatching, ]]>
F3 eggs deposited by P. columella fed with spirulina. Evidently, adults fed with spirulina were able to produce better quality eggs with higher survival rates, which results in a higher number of viable offspring. ]]>
P. columella snails fed with lettuce plus spirulina showed a higher survival rate and a higher growth increment during their whole life, but especially on the first months of life (30-60 dpl). Newly-hatched snails usually remain attached to the bottom of the glass aquarium, exactly where the spirulina was settled, and probably served as their primary food source. Hatchlings do not usually come to the water surface, where ]]>
P. columella. When this critical ]]>
P. columella snails fed without spirulina showed higher mortality rates, and those that survived had a slower growth increment, and equal the size of P. columella snails fed with spirulina after 180 dpl.
As mentioned before, the quality of the diet provided as food for raising lymnaeid snails under laboratory conditions had a significant effect on their growth, fecundity and fertility, as well-fed snails became larger and laid more eggs (Rondelaud et al., 2004). Several studies have demonstrated that food ]]>
P. columella, as the individuals fed with this combination showed bigger sizes, faster growth rates, become sexually mature early ]]>
P. columella fed with this alga. Snails fed with spirulina enhanced significantly their fitness parameters. ]]>
Another factor that must be taken into account is the effect of spirulina on water quality. Although in both treatments the water was suitable for P. columella maintenance, the supplementation with spirulina improves the quality of the water. In the glass aquarium with spirulina the water was much harder ]]>
P. columella, which spend their entire life without rising to the surface, require higher concentrations of dissolved oxygen in the water to breathe (Cuezzo, 2009). Accordingly, higher levels of dissolved oxygen in the water will improve the development of P. columella, as was observed. High levels of ]]>
P. columella in a direct and in an indirect way; in the former case by consuming it and in the latter by improving the water quality.
Only a few ]]>
P. columella under laboratory conditions (León-Dancel, 1970; Souza, & Magalhães, 2000), and in all of them, snails were reared and maintained under very different conditions of temperature, food, substratum, photoperiod, etc. As was already stated, growth, fecundity, fertility and survival are affected by these variables (Islam et al., ]]>
In conclusion, this study has been novel in demonstrating the benefits of using spirulina as a food source for rearing P. columella
in the laboratory. We provided evidence that the supplementation of P. columella diet with commercial spirulina enhances it fitness and improves the artificial breeding of the species. The present study is the first to reveal the benefits of incorporated spirulina as a food source for breeding
P. columella (and other Lymneids) snails in laboratory. Snails fed with spirulina showed enhanced fitness parameters showing higher survival and growth rates, smaller size at first reproduction, longer reproductive period and enhanced lifetime fecundity and offspring viability. The aquaculture breeding technique described here is strongly recommended for breeding this species, because it will provide large numbers of reproducing adults and viable offspring that can be used in future biological assays to provide accurate information on some biological aspects of P. columella, such as, how long can these snails live, what is the relationship between size and age, at what size does egg-laying begin and finish and what is the duration of their reproductive life.
Acknowledgments
We thank Claire Standley of Princeton University for her valuable comments on the manuscript and José Alvarez of Universidad Nacional del Nordeste (UNNE) for his field assistance. This research was supported by grants from Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina (CONICET, PIP 0821) and Agencia Nacional de Promoción Científica y Tecnológica, Argentina (ANPCYT, PICT 00031).
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1. Unidad de Ecología de Reservorios y Vectores de Parásitos - Instituto de Ecología, Genética y Evolución de Buenos Aires - IEGEBA (CONICET-UBA), Departamento de Ecología, Genética y Evolución (FCEN-UBA), Intendente Güiraldes 2160, Pabellón 2, Laboratorio 55, CP C1428EGA, Ciudad Autónoma de Buenos Aires, Argentina; lucilap@ege.fcen.uba.ar, jpujadas@ege.fcen.uba.ar, criswi@ege.fcen.uba.ar
Received 13-VIII-2014. Corrected 30-X-2014. Accepted 26-XI-2014.