Size Variation of Morphological Traits in Bosmina Freyi and Its Relation with Environmental Variables in a Tropical Eutrophic Reservoir

Size variation of morphological traits in Bosmina freyi and its relation with environmental variables in a tropical eutrophic reservoir

RESEARCH / INVESTIGACIÓN Size variation of morphological traits in Bosmina freyi and its relation with environmental variables in a tropical eutrophic reservoir

Yury Catalina López-Cardona1, Edison Parra-García1, Jaime Palacio-Baena2, Silvia Lucía Villabona-González3 DOI. 10.21931/RB/2021.06.02.16 Abstract: We assessed the size variation of morphological traits in Bosmina freyi regarding changes in environmental variables, the biomass of invertebrate predators, and algal food availability in two depths of the photic zone, the riverine zone, and near the dam zone (lacustrine zone) in The Riogrande II reservoir. In 200 individuals of B. freyi, using the software TpsDig2 we measured the body size, mucron and antennule lengths, and the antennule aperture percentage. Using the Mann-Whitney U test, we assessed the differences between these traits considering the zones and the photic depths; however, we used a 1763 canonical discriminant analysis with morphologic traits and environmental variables. Measured morphological traits showed a heterogeneous distribution between sampled zones and depths (p < 0.05). The highest values mucron and antennule lengths and the smallest antennule aperture angle were observed on small body size individuals, associated with physical, chemical, and biological characteristics in the riverine zone and the subsurface. Size structure distribution in B. freyi was related to changes in water temperature, trophic state, depredation, availability, and quality of food, of which implications related to the zooplankton community structure, predator-prey relations, and energy flow in the reservoir.

Key words: Cladocera, predation, size structure, trophic state.

Introduction Methods Cladocera is a zooplankton assemblage that occupies an The Riogrande II reservoir is located in the northeastern of intermediate position in the aquatic food chain1 because they Colombia in The Río Grande II basin at 2200 m.a.s.l (6º 33' 50"- ingest protozoa2, algae, bacteria, and detritus lentic systems, 6º 28' 07" N and 75º 32' 30"- 75º 26' 10" O). Has a total volume and simultaneously they constitute one of the chosen prey for up to landfill level (2270 m.a.s.l) of 240 million of 3m and an invertebrates and vertebrates3. average area of 1214 ha. This waterbody receives water from Some species of this group have a wide variation in size the Grande and Chico rivers and the Las Ánimas creek19. This structure due to genetic factors4 and environmental factors as system is mainly used for hydroelectric generation and potable temperature5, food availability6, pH7, and acidification1. water supply20. The Riogrande II reservoir has higher turbidity Bosmina genera is a group of small cladoceran filter fee- and a greater degree of eutrophication at riverine zones, main- ders8 with variations in body size, shape, and length of anten- ly in the Chico River zone, due to sediment washing process in nules and mucron1,5,9. the basin and the domestic, industrial, agricultural, and livestock According to Masson S (2004)10 in Canadian lakes, increa- wastewater discharge from the closer cities (Entrerríos and San sing chlorophyll-a concentrations favors small individuals' Pedro de los Milagros) located in the two principal rivers21. predominance. Other authors detail that some changes in This research was conducted as part of the “Estudio de la Bosmina size are because the predation pressure by Copepo- problemática ambiental de tres embalses de Empresas Públi- da, Rotifera11,12 and macroinvertebrates of Chaoborus gene- cas de Medellín para la gestión integral y adecuada del recurso ra1,4,8,9,13, indicate that predation by invertebrates induces an hídrico”, we carried out five sampled areas in The Riogrande II increase of size and the development of defense structures as reservoir, in the subsurface and the photic zone edge (Figure 1) the elongation of mucron and antennules in Bosmina. in September 2011. The highest dominance of Bosmina freyi Bosmina freyi14 contributes more than 60% of the total happened in this period15. zooplankton biomass in The Riogrande II reservoir15 due to its Physical, chemical and biologic variables data information broad trophic plasticity16 and resistance to high turbidity con- (chlorophyll-a and plankton biomass) were took from the “Es- ditions17. This species was reported for the first time in 2004 in tudio de la problemática ambiental de tres embalses de Em- South-America18, for Colombia in 2010 (Elmoor-Loureiro, com. presas Públicas de Medellín para la gestión integral y adecua- pers.), and consequently, there is a lack of information about da del recurso hídrico”15,22-24. the structure of morphological traits. Methods for zooplankton sample collection and the esti- We hypothesized that if the size distribution of morpholo- mation of Carlson index of trophic state (TSI) modified by (25) gical traits of Bosmina freyi in the vertical and longitudinal axis are described in (14). in The Riogrande II reservoir changes concerning environmen- We took 20 specimens of B. freyi (n = 200 individuals), tal variables and the presence of invertebrate predators, so in and we used a photographic camera adapted to an optical the reservoir zone with the highest trophic state and warmer microscope and were individually photographed to determine water, individuals of small size will dominate and in zones with morphological traits using TpsDig2 (Figure 2). Lengths were high invertebrate predators biomass, individuals will have a measured in µm and the antennule angle in the opening per- mucron and antennule with a longer length and an antennule centage, assuming that a right angle (90°) has an aperture of closed-angle. 100%. 1 Grupo de Investigación en Limnología Básica y Experimental y Biología y Taxonomía Marina, Universidad de Antioquia, Medellín, Colombia. 2 Grupo de Investigación en Gestión y Modelación Ambiental, Universidad de Antioquia, Medellín, Colombia. 3 Grupo de Investigación en Limnología y Recursos Hídricos, Universidad Católica de Oriente, Rionegro, Colombia.

Corresponding author: [email protected] Yury Catalina López-Cardona, Edison Parra-García, Jaime Palacio-Baena, Silvia Lucía Villabona-González Volumen 6 / Número 2 • http://www.revistabionatura.com

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Figure 1. Study area and location of sampling stations. Data analysis We used a Mann–Whitney U test because data did not fulfill the normality of residuals and homogeneity of varian- ces. The last is to assess the significance of the differences between individuals' morphological traits from the zones and depths. We also made a Generalized Discriminant Analysis using the measured morphological traits and the environmental variables. We calculated the scores and canonical vectors for graphic representation of the essential canonical discriminant functions in terms of explained variance, allowing a simple interpretation in the canonical space of differentiation among morphological traits of B. freyi and the environmental matrix26. Data analyses were made using R Wizard V 2.3 Software27.

Figure 2. Body length (BL), mucron length (ML), antennule Results total length (AL) and antennule angle (AA) of Bosmina freyi The riverine zone had the highest temperature degree, (Modified from (5)) greater eutrophication, and higher phytoplankton biomass Size variation of morphological traits in Bosmina freyi and its relation with environmental variables in a tropical eutrophic reservoir

(chlorophyll-a), rotifers (Asplanchna girodi De Geurne, 1888), body size and antennule aperture were mainly associated with and copepods predators (Mesocyclops longisetus Thiébaud, the photic zone boundary, with higher predatory copepods and 1912; Metacyclops leptopus Kiefer, 1927; and M. mendocinus rotifers biomass, as well as phytoplankton and Cryptomonas Wierzejski, 1892) biomass. Meanwhile, the lacustrine zone re- sp. biomass (Figure 4 b & 5). corded the highest transparency, dissolved oxygen concentration, and Cryptomonas sp. biomass (Table 1). B. freyi body length varied over the range of 202.64 and Discussion

457.02 µm (average = 294.7 µm), mucron length between 28 14.87 and 29.94 µm (average = 22.47 µm), antennule length Melão, M. G. (1999) mentioned that temperature increa- between 94.21 and 170.25 µm (average = 134.11 µm) and the se is a factor that directly affect organism's life cycle and po- antennule opening angle ranged between 72.48 and 88.21% pulation attributes, causing a time decrease in the organism's growth and an increase in population growth rates, which fa- (average = 81.05%). 29 According to the Mann-Whitney U test, mucron and an- vors large populations with small size individuals , such as we tennule lengths and the opening angle were significantly di- observed in this study in the riverine zone and in the reservoir subsurface, where occurred the highest number of individuals 1765 fferent among sampling zones and depths (Figure 3, a & b). 30 Meanwhile, body length was significantly different among dep- with youth traits and higher mucron and antennule lengths . a ths; it exhibited a significantly higher value in the specimens Higher values of Carlson Index (TSI) and chlorophyll- from the photic zone boundary (Figure 3 b). While mucron and concentration in the riverine zone also favor small individuals antennule lengths were higher in individuals from the riveri- due to a continuous energy source to maintain high metabolic 31 B. freyi ne zone and the subsurface concerning those from the lacus- rates . So, population size structure in the reservoir trine zone and the photic zone boundary, antennule aperture seems to behave similarly to the general pattern of cladoceran size structure, in which smaller species are correlated to con- showed an opposite behavior. 32 A variance of 100% explains canonical discriminant analy- ditions of a more significant trophic state . sis among zones and depths in the first axis. In both cases, It has been reported that biotic variables have an indirect classification and cross-validation values were 100%, clearly influence on mucron and antennule sizes and a direct effect on spatial and temporal population's dynamic, affecting the discriminating between riverine zones and lacustrine zone, as 33 well as the subsurface and the photic zone boundary. presence of predators and establishing food restrictions . This situation implies changes in size structure and the lengths of While individuals of B. freyi with higher mucron and anten- 1 nule lengths are related with the riverine zone (warmer waters, species attributes , as evidenced by this study. as well as a greater degree of eutrophication and higher phyto- The highest biomass of predatory copepods and rotifers in plankton and predatory copepods biomass), in the lacustrine the riverine zone matched with has been reported in some stu- zone (more oxygenated and clear waters), specimens showed dies about the influence of predation by invertebrates on mor- Bosmina 9,34,35 36 a tendency to present higher body size and an antennule more phological traits of genera . Significantly , claim separated from the body (Figure 4 a & 5). that copepods can consume Bosminidae species with sizes Depths were discriminated mainly by the presence of in- less than 400 µm. Nevertheless, the highest mucron and an- dividuals with a higher mucron and antennule lengths in the tennule size could reduce predation rates of small individuals of B. freyi by copepods, as it happens with other cladoceran subsurface, related to a higher temperature and greater dis- 37 solved oxygen availability. By contrast, individuals with higher species .

Figure 3. Morphological traits distribution BL, ML, AL, and AA into two zones (a) and depths (b) in the photic zone of The Rio- grande II reservoir, September 2011. Yury Catalina López-Cardona, Edison Parra-García, Jaime Palacio-Baena, Silvia Lucía Villabona-González Volumen 6 / Número 2 • http://www.revistabionatura.com

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Table 1. Physical, chemical, and biological variables in The Riogrande II reservoir's photic zone, September 2011. C.V (%) = Coefficient of Variation.

Antennule aperture may also be a defense mechanism cies subsurface. This could resemble the vertical distribution of against predators, and it depends on the predator attack me- sizes in B. freyi population in which the individuals of larger size chanism. Some authors such as (38, 39) consider that a curved and smaller antennule and mucron length were mainly concen- antennule (lower aperture) as that of the individuals detected trated in the deepest layer of the photic zone. in the riverine zone, protects the ventral part of cladocerans Predatory copepods and rotifers agglomerated in this la- from some predators of genus Mesocyclops and especially yer, and probably, as the individuals of B. freyi with a larger size from Asplanchna girodi, a rotifer species that dominated the (higher than 400 µm), they avoid predation/or are selectively biomass of rotifers in The Riogrande II reservoir during the removed from the subsurface15. study made by (15). The highest abundance of more significant individuals and The highest biomass of the smaller organisms of B. freyi, smaller mucron and antennule lengths tended to coincide with of the predatory copepods and rotifers, may also be due to the the increase of Cryptomonas sp biomass in the zone near the highest primary production in the riverine zone40 because the dam (lacustrine zone), the photic zone boundary. The last im- highest availability of resources may determine its presence plies that maybe these genera of algae constitute an essen- in the longitudinal axis of the reservoir through the tributaries, tial resource for adults of B. freyi30 in the reservoir24 said that especially the Chico River39. nanoplanktonic and mixotrophic species of Cryptophyta are a In the vertical axis, the size distribution of B. freyi structures persistent component of zooplankton diet from The Riogrande could be attributed to vertical migration, common in the zoo- II reservoir; apparently, it favors its growth and reproduction planktonic community, particularly in Bosmina genera41. In The rates because it provides enough organic carbon, nitrates, and Riogrande II reservoir15 found a gradient in the vertical distribu- phosphates. Furthermore, it is very feasible that B. freyi com- tion of the zooplankton biomass. While smaller species seem to plements its diet with detritus42 and that alimentary strategy prefer superficial layers of the reservoir, the largest ones tend to becomes more critical on small individuals of B. freyi together be located in the deepest layers of the photic zone, probably as a with the dissolved substances and organisms of picoplankton strategy to avoid predation and selective removal of bigger spe- ingestion (< 2 µm). Size variation of morphological traits in Bosmina freyi and its relation with environmental variables in a tropical eutrophic reservoir

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Figure 4. Canonical Discriminant Analysis applied to B. freyi morphological traits, environmental variables and phytoplankton, and zooplankton biomass. Linear regression model for zones (a) and depths (b) in the photic zone of The Riogrande II reservoir, September 2011.

Conclusions Results showed that the distribution in the size structure Consequently, the distribution of the size structure of B. in B. freyi is related to changes in biotic and abiotic variables. freyi affects the structure of the zooplanktonic community, So, high temperatures and a greater nutrients concentration the predator-prey trophic relationships, and the flow of energy favored the growth of small individuals' populations, mainly in and matter in the reservoir. Nevertheless, factors do not invol- the reservoir's riverine zones. ve here, as competence and seasonality may also be determi- Small sizes individuals seem to be protected from preda- nants and affect the population attributes of B. freyi. tion by other zooplankters as rotifers and copepods by a high mucron and antennule length, as well as by a closed antennu- Acknowledgments le. By contrast, individuals from B. freyi with a bigger size and Thanks to the program “Estudio de la problemática am- adult features just like predatory rotifers and copepods seem biental de tres embalses de Empresas Públicas de Medellín to avoid predation pressure, probably from visual predators as para la gestión integral y adecuada del recurso hídrico”, for the vertebrates, remaining mainly in the deepest zone of the photic provision of information; and to the research groups Limno- layer. Furthermore, these cladocerans coexist with the highest base-Biotamar and GAIA from the Universidad de Antioquia densities of Cryptomonas sp., one of the most nutritious re- for their support. Thanks to Isabel Cristina Gil for the paper sources for Bosmina in the reservoir. translation. Yury Catalina López-Cardona, Edison Parra-García, Jaime Palacio-Baena, Silvia Lucía Villabona-González Volumen 6 / Número 2 • http://www.revistabionatura.com

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Figure 5. Distribution map of size variation of morphological traits in Bosmina freyi in The Riogrande II reservoir.

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