Animal Biology 67 (2017) 331–338 brill.com/ab

Short Note

Null models for understanding fairy shrimp habitats

Patricio De los Ríos Escalante1,2,∗ 1 Universidad Católica de Temuco, Facultad de Recursos Naturales, Escuela de Ciencias Ambientales, Casilla 15-D, Temuco, Chile 2 Núcleo de Estudios Ambientales, UC Temuco, Chile Submitted: March 10, 2017. Final revision received: July 26, 2017. Accepted: August 19, 2017

Abstract The Chilean fairy shrimp species are represented by the Branchinecta genus, which are poorly de- scribed, and mainly occur in shallow ephemeral pools in the Atacama Desert of northern Chile and the Southern Chilean Patagonian plains. The aim of the present study was to perform an initial ecolog- ical characterization of Branchinecta habitats and its associated communities in the Chilean Southern Patagonian plains (45-53°S) using null models (co-occurrence, niche sharing and size overlap). The results of the co-occurrence analysis revealed that the species’ associations are structured, meaning that at different kinds of Branchinecta habitats, the associated species are different. I did not find niche sharing, which means interspecific competition is absent. Finally the size overlap analysis revealed structured patterns, which are probably due to environmental homogeneity or colonization extinction processes. The habitats studied are shallow ephemeral pools, with extreme environmental conditions, where continuous local colonization and extinction processes probably occur, which would explain the marked Branchinecta species endemism.

Keywords Branchinecta; colonization; crustaceans; endemism; extinction; niche sharing; null models; Patagonia

Introduction

Relatively little is known about the Chilean fairy shrimps because studies have mainly focused on the occurrence of these species, which belong to the Branchinecta Verrill, 1869 genus (De los Ríos-Escalante et al., 2013; De los Ríos- Escalante & Kotov, 2015). These species were described originally for shallow low salinity ephemeral pools in northern Chile (20-22°S; Rogers et al., 2008) and would probably be useful indicators of low salinity and oligotrophic shallow ephemeral

∗ ) E-mail: [email protected]

© Koninklijke Brill NV, Leiden, 2017 DOI 10.1163/15707563-00002532

Downloaded from Brill.com09/24/2021 07:54:44PM via free access 332 P. De los Ríos Escalante / Animal Biology 67 (2017) 331–338 pools located in southern Patagonian plains (45-53°S; De los Ríos et al., 2008). Cur- rently, there are seven confirmed Branchinecta species, nevertheless these are not reported for South America (IUCN, 2017). However, from a biogeographical view point, in southern Patagonian these shrimps would be expected to show continuous colonization and extinction dynamics due to the presence of many ephemeral pools that would also explain the high crustacean species endemism and richness there (Menu-Marque et al., 2000; De los Ríos-Escalante & Robles, 2013). The Branchinecta habitats in Chile are characterized by an absence of fish, and are nesting and feeding sites for aquatic birds such as swans, flamingoes and ducks (Soto, 1990; De los Ríos-Escalante, 2010). According to the literature descriptions, Branchinecta in southern Patagonian habitats have a detritivorous diet, consuming mainly dead plant material and grazing on periphyton (Paggi, 1996; Pociecha & Dummont, 2008). They probably have no competitor species, because other mi- crocrustacean species such as copepods of the Boeckella genus and cladocerans of the Daphnia genus graze mainly on phytoplankton and bacteria, and the poten- tial predator would be the large-bodied copepod Parabroteas sarsi Mrázek, 1901 (De los Ríos-Escalante, 2010). Given the limited information available about these species, the aim of the present study was to provide ecological descriptions, based on null model analysis, of crustacean species communities in fairy shrimps habitats in Southern Chilean Patagonia.

Material and methods Field work Data were collected during field work done in 2001, 2002 and 2006 on sites with shallow ephemeral pools (surface z 1 km2 and maximum depth < 1) in Patagonian plains. There sites were located in Balmaceda (45°53S; 71°40W), two sites at Vega del Toro (51°07S; 71°40W) and seven sites at Kon Aiken (52°50S; 72°10W). These ephemeral pools are only present in early southern spring (September- October) and have low conductivity (0.42-0.70 mS/cm) and chlorophyll concen- tration (2.1 to 4.4 mg/L; De los Ríos et al., 2008). Samples were collected using horizontal hawls with a plankton net of 20 cm diameter and 80 μm mesh size. Crus- tacean zooplankton specimens were identified using literature descriptions (Araya & Zúñiga, 1985; Bayly, 1992; Rogers et al., 2008) and species percentage was es- timated for data collected in 2001 and 2002. Also presence-absence data obtained during field work in 2001, 2002 and 2006 were considered (De los Ríos et al., 2008).

Data analysis A species’ absence/presence matrix for all available data was constructed, with the species in rows and the sites in columns (table 1). I calculated a Checkerboard score (“C-score”), which is a quantitative index of occurrence that measures the extent to which species co-occur less frequently than expected by chance (Gotelli, 2000).

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Table 1. Presence-absence species matrix for sites during the studied period. Codes for studied sites: B1, B2 and B3: Balmaceda 1, Balmaceda 2, Balmaceda 3 (collection date: September 2001); V1 and V2: Vega del Toro 1 and Vega del Toro 2 (collection date: October 2002); K1 to K7: Kon Aiken 1 (Collection date: October 2002); Kon Aiken 2, Kon Aiken 3, Kon Aiken 4, Kon Aiken 5, Kon Aiken 6, and Kon Aiken 7 (collection date: October 2006).

B1 B2 B3 V1 V2 K1 K2 K3 K4 K5 K6 K7

Anostraca Branchinecta gaini Daday, 1902 1 1 11111 B. granulosa Daday, 1902 1 1 B. vuriloche Cohen, 1985 1 1 1 Cladocera Daphnia ambigua Scourfield, 1947 1 1 D. dadayana Paggi, 1999 1 1 1 11111 D. pulex (De Geer, 1778) 1 1 Chydorus sphaericus (O. F. Müller, 1785) 1 1 Copepoda Boeckella brasiliensis (Lubbock, 1885) 1 B. gracilipes Daday, 1901 1 1 1 B. michaelseni Mrázek, 1901 1 B. poppei, Mrázek, 1901 1 1 1 1 1 11111 Parabroteas sarsi Mrázek, 1901 1 1 111111111 Cyclopoida 1 1 1 Nauplius 1 1 1

A community is structured by competition when the C-score is significantly larger than expected by chance (Gotelli, 2000; Tondoh, 2006; Tiho & Johens, 2007). In addition, I compared co-occurrence patterns with null expectations via simulation. Gotelli & Ellison (2013) suggested the statistical null model Fixed-Fixed: in this model the row and column sums of the matrix are preserved. Thus, each random community contains the same number of species as the original community (fixed column), and each species occurs with the same frequency as in the original com- munity (fixed row). The null model analyses were performed using the software “R” (R Development Core Team, 2009) and the package EcosimR version 7.0 (Gotelli & Ellison, 2013; Carvajal-Quintero et al., 2015). Percentage data were considered based on information collected in field work data from 2001 and 2002 (table 2), and a niche sharing null model was applied using Pianka’s overlap index with retained niche breadth and reshuffled zero states using the Ecosim version 7.0 software (Gotelli & Ellison, 2013; Carvajal-Quintero et al., 2015). The Ecosim program also determines whether measured overlap values dif- fered from what would be expected in random sampling of the species data. Ecosim performs Monte Carlo randomisations to create pseudo-communities and then sta- tistically compares the patterns of these randomised communities with those in the

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Table 2. Percentage of abundances of Chilean Patagonian fairy shrimp’s habitats. Codes for studied sites: B1, B2 and B3: Balmaceda 1, Balmaceda 2, Balmaceda 3 (collection date: September 2001); V1 and V2: Vega del Toro 1 and Vega del Toro 2 (collection date: October 2002); K1: Kon Aiken 1 (collection date: October 2002).

B1 B2 B3 V1 V2 K1

Anostraca B. gaini 4.1 B. granulosa 2.56.7 B. vuriloche 1.01.31.9 Cladocera D. ambigua 4.66.7 D. dadayana 7.440.0 D. pulex 4.813.3 Ch. sphaericus 1.76.5 Copepoda B. brasiliensis 28.0 B. gracilipes 65.743.316.730.9 B. michaelseni 1.3 B. poppei 9.84.683.723.7 P. s a rs i 8.944.41.333.341.2 Cyclopoida 15.08.99.3 Nauplius 6.99.611.1

real data matrix (Gotelli & Ellison 2013). In this analysis all values of the gen- eral matrix were randomised 1000 times and the niche breadth was retained for each species. In other words, the algorithm retained the amount of specialization for each species (Gotelli & Ellison, 2013; Carvajal-Quintero et al., 2015). Finally for data collected in field work during 2006, I measured total length con- sidering the distance from head to the furcae basis for ten individuals of each species observed in two sites (De los Ríos-Escalante, 2012a). To these data, a size overlap null model analysis was applied, with the aim of determine the non-random pat- terns in size overlap using the software EcosimR (Gotelli & Ellison 2013; Ward & Beggs, 2007). For this purpose, a matrix with one row for species and a second row for size length average was made, the original matrix was reordered for originate random patterns that would generate interspecific competence absence. I applied the following option: length segment variance with metric size overlap, because this uses the mean observation trend; in a structured assemblage this would have a low variance in comparison to random assemblage. Also, I performed a logarith- mic transformation that can be necessary in case of large size difference between species (Gainsbury & Colli, 2003).

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Results and discussion The species assemblages revealed that species from the Branchinecta genus have a relatively high crustacean species richness, where the coexistence with cladocerans of the Daphnia genus, copepods of the Boeckella genus, and the presence of the predator Parabroteas sarsi is possible (tables 1 and 2). The results of the species co-occurrence null model analysis revealed that species associations are markedly structured (table 3), whereas no niche overlap was revealed that would imply the absence of competition between species (table 3). Finally, the size overlap analysis revealed no interspecific competition (tables 3 and 4). My results agree with descriptions of the species associated with the Branchinecta genus on sub-Antarctic islands (Hansson et al., 1996). In accordance with the literature, these sites have high species richness with marked environmen- tal heterogeneity (Pugh et al., 2002; Dartnall, 2005). The reports also indicate that the Branchinecta genus in southern Patagonian plains is associated with low con- ductivity and oligotrophic water bodies (De los Ríos et al., 2008). Although the

Table 3. Results of species co-occurrence, niche sharing and size overlap null models analyses.

Observed Mean of Variance of P index simulated index simulated index ∗ Species co-occurrence 5.296 3.991 0.015 <0.001 ∗∗ Niche sharing 0.555 0.389 0.002 0.002 ∗∗∗ Size overlap (K1) 1.346 27.671 1219.000 0.944 ∗∗∗ Size overlap (K2) 1.400 20.413 602.760 0.912

∗ ∗∗ Symbols: Analysis based on all data collected in 2001, 2002 and 2006; Analysis based on data ∗∗∗ collected in 2001 and 2002; Analysis based on data collected in 2006.

Table 4. Size length (average in mm ± standard deviation) for crus- tacean species observed in Kon Aiken shallow ephemeral pools sites 2 and 3 (from data collected in 2006).

K1 K2

Anostraca B. gaini 20.1 ± 2.120.1 ± 2.1 Cladocera D. dadayana 1.9 ± 0.81.5 ± 0.6 Copepoda B. poppei 3.7 ± 1.51.8 ± 0.7 P. s a rs i 5.1 ± 0.25.0 ± 0.3

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Branchinecta genus is absent in northern Patagonian shallow pools, their zooplank- ton community structure is similar to Branchinecta habitats that can also harbor non selective grazers such as cladocerans (Daphnia), selective grazers such as copepods (Boeckella), and large-bodied predators (Parabroteas sarsi: Modenutti et al., 1998; De los Ríos-Escalante, 2010, 2012b). From a biogeographical point of view point, the reported species produce rest- ing stages when environmental conditions are not favorable. These resting forms configure the resting egg bank that would generate an advantage for colonizing new habitats (Adamowicz et al., 2002, 2007; Aleeksev, 2007a, b, 2010; Aleeksev et al., 2007). In this scenario, the presence of continuous colonization and extinction processes at local spatial scale would explain the species heterogeneity found for the studied sites. When expressed in structured species associations, this scenario would also be supported by biogeographical evidence, because southern Patagonia is a zone with high crustacean species richness and endemism (Adamowicz et al., 2002, 2007; Menu-Marque et al., 2000). The results of niche sharing and the absence of competition between species would also agree with literature descriptions of such absence of competition in trophic interactions between zooplankton species in shallow Patagonian plains (Balseiro & Vega, 1994; Vega, 1995, 1997, 1998, 1999; Dieguez & Balseiro, 1998; Brandl, 2005) and large and deep north Patagonian lakes (De los Ríos-Escalante & Woelfl, 2017). In this respect, the crustacean zooplankton species seem to have niche segregation in term of grazing activity (De los Ríos-Escalante & Woelfl, 2017). On the basis of the null models considered in the present study, the interactions that involve crustacean zooplankton in Branchinecta habitats are suggested to have marked niche specialization. Specifically, species co-occurrence reveal the specific composition in term of species, and the other two null models for niche sharing and size overlap indicate the absence of competition due to niche specialization. To conclude, more studies focusing on fairy shrimp habitats in Chilean Patagonia, considering their ecological role in crustacean communities and predator-prey in- teractions with the other species included in the community are now needed.

Acknowledgements The present study was funded by the project Tides Grant Foundation TRF13-03011 MECESUP UCT 0804 and the Research Direction of the Catholic University of Temuco. I am grateful to M.I. and the Editor-in-Chief for their valuable comments that helped improve a previous version of this manuscript.

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