African Journal of Aquatic Science

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Habitat utilisation of afer and capensis in headwaters of the Swartkops River, Eastern Cape, South Africa

B Hannweg , SM Marr , LE Bloy & OLF Weyl

To cite this article: B Hannweg , SM Marr , LE Bloy & OLF Weyl (2020): Habitat utilisation of Pseudobarbus￿afer and Sandelia￿capensis in headwaters of the Swartkops River, Eastern Cape, South Africa, African Journal of Aquatic Science, DOI: 10.2989/16085914.2020.1719815 To link to this article: https://doi.org/10.2989/16085914.2020.1719815

Published online: 12 Jun 2020.

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Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=taas20 African Journal of Aquatic Science 2020: 1–9 Copyright © NISC (Pty) Ltd Printed in South Africa — All rights reserved AFRICAN JOURNAL OF AQUATIC SCIENCE This is the final version of the article that is published ISSN 1608-5914 EISSN 1727-9364 ahead of the print and online issue https://doi.org/10.2989/16085914.2020.1719815

Habitat utilisation of Pseudobarbus afer and Sandelia capensis in headwaters of the Swartkops River, Eastern Cape, South Africa

B Hannweg1,2, SM Marr2,3* , LE Bloy1,2,3 and OLF Weyl2,3,1

1 Department of Ichthyology and Fisheries Science, Rhodes University, Makhanda, South Africa 2 DSI/NRF Research Chair in Inland Fisheries and Freshwater Ecology, South African Institute for Aquatic Biodiversity, Makhanda, South Africa 3 Centre for Invasion Biology, South African Institute for Aquatic Biodiversity, Makhanda, South Africa *Correspondence: [email protected]

Habitat degradation is one of the greatest threats to endemic freshwater in the Cape Fold Ecoregion. One habitat restoration strategy is the replication of critical habitat using artificial materials. In this paper, we evaluate the habitat occupancy of two small, endemic headwater fish of the Cape Fold Ecoregion, namely the Eastern Cape redfin Pseudobarbus afer (Peters, 1864) and the Cape Kurper Sandelia capensis (Cuvier, 1829). Habitat occupancy was observed in five pool microhabitats (inflow, woody debris, deep open, fern-root wads, and outflow) using action cameras. Changes in habitat occupancy were assessed following the introduction of an artificial habitat in the form of PVC pipes. Pseudobarbus afer preferred deeper open habitats, whereas Sandelia capensis preferred more structured woody debris habitat. Habitat occupancies differed significantly across all microhabitats for both ; excluding those between the inflow and outflow, and the open deep and fern-root wads for Sandelia capensis. Pseudobarbus afer and S. capensis occupancies in the natural microhabitats reduced significantly following the introduction of the artificial habitat. For species restricted to degraded habitats that require habitat restoration, the use of artificial habitat may be beneficial in accelerating the recovery of such species.

Keywords: action cameras, artificial habitat, conservation, endangered fish, headwater streams, maxN, proportional occupancy

Supplementary material: available online at https://doi.org/10.2989/16085914.2020.1719815

Introduction

Globally, freshwater ecosystems are facing a variety of 2008); e.g. food, shelter, predator avoidance, breeding human-mediated threats and a large number of species are habitat, etc. (Odling-Smee et al. 2011). Therefore, at risk of population declines towards extinction (Darwall conservation strategies for species at risk must protect or et al. 2018). Threats, including habitat degradation/ restore specific habitats within water bodies, especially fragmentation/alteration and siltation, water pollution, critical habitats (Rosenfeld and Hatfield 2006), and the overabstraction and flow modification, and the introduction connectivity between these habitats. However, habitat of non-native fish species (Darwall et al. 2018), are requirements through the entire life cycle of most fish are compounded for species isolated within headwater streams poorly understood (Fausch et al. 2002) and understanding or with restricted geographical distributions (Ellender et the association between habitat and the wellbeing of fish al. 2017). The Cape Fold Ecoregion, sensu Abell et al. populations is required for efficient, effective conservation (2008), is a hotspot of endemism and threatened freshwater or restoration strategies (Rabeni and Sowa 1996). fish species in southern Africa (Tweddle et al. 2009). One approach to restoring habitat is the replication of The greatest threats to the fish of this ecoregion are the the natural habitat using artificial materials (Seaman and presence of non-native fish species and habitat degradation Sprague 1991). Globally, artificial structures have been (Tweddle et al. 2009; Ellender et al. 2017). Although deployed in marine and freshwater systems to create projects to address the threats of non-native fish have been habitat for a variety of aquatic organisms (Seaman and executed (Weyl et al. 2014; Shelton et al. 2017; van der Sprague 1991). Artificial habitats can be used as freshwater Walt et al. 2019), restoration of riverine habitat has received fish conservation measures to boost population numbers less attention. There is, therefore, a requirement to start by providing habitats important to their specific life histories researching the restoration of riverine habitat for the fish of (Schlaepfer et al. 2005; Yokomizo et al. 2007; Westhoff et the Cape Fold Ecoregion. al. 2013). Fish have been found to utilise artificial habitats Habitat requirements of fish species are dependent on for refuge or foraging in situ (Clark and Edwards 1999; Pratt their specific life-cycle stage (Schlosser 1991) and their et al. 2005; Santos et al. 2008) and in the laboratory (Kadye specific requirements in each life stage (Orpwood et al. and Booth 2014; Magellan and García-Berthou 2015).

African Journal of Aquatic Science is co-published by NISC (Pty) Ltd and Informa UK Limited (trading as Taylor & Francis Group) Published online 12 Jun 2020 2 Hannweg, Marr, Bloy and Weyl

Fish habitat analysis in streams can be conducted at of the Swartkops River, Eastern Cape, South Africa, in two complementary levels: 1) behavioural associations of the Groendal Wilderness Area. The Fernkloof River lies individuals at a microhabitat scale, and 2) associations of entirely within the Groendal Wilderness Area and has been populations with larger-scale habitat elements (Rabeni minimally impacted by human activities. Sites comprised and Sowa 1996). Population-level analysis highlights the of four pool habitats selected on the basis of the presence importance of fluvial dynamics, whereas microhabitat of the target species, having suitable water clarity for analysis highlights local scale habitat elements that could underwater photography, and containing the five selected explain fish abundance and distributions (Rabeni and Sowa microhabitats: inflow (shallow, fast, turbulent water at the 1996). This paper aims to conduct a microhabitat analysis head of the pool), outflow (shallow, slow water at the tail of for two small, endemic, headwater fish species, Eastern the pool), deep open (open water at the deepest point in the Cape redfin Pseudobarbus afer (Peters, 1864) and Cape pool), woody debris (branches and twigs in the pool) and Kurper Sandelia capensis (Cuvier, 1829), in the field using fern-root wads (each pool had a rock face on one bank that an underwater-camera array to (1) demonstrate the use had ferns growing on the waterline with their root wads in of action cameras to determine the habitat occupancy; (2) the water). assess the differences in the habitat occupancy for each Water physico-chemical parameters, pH, temperature of the species; (3) assess the difference in the habitat (°C), and electrical conductivity (µs cm−1), were measured occupancy between the two species and (4) assess using a HANNA HI98129 combo probe (HANNA the change in the habitat occupancy of the two species Instruments, Inc., United States of America.). A portable following the introduction of an artificial habitat. The HANNA HI 98703 turbidity meter (HANNA Instruments, Inc., two species co-occur throughout the P. afer distribution United States of America.) was used to measure turbidity range, and S. capensis co-occurs with Pseudobarbus (NTU). Three measurements of each parameter were species throughout its distributions range. Both species recorded at the inflow, deep open, and outflow sites of each occur predominantly in pools although P. afer frequently pool and averaged for the visit. forage in riffles (Skelton 2001). Although some research has been conducted on the breeding behaviour of both Baseline habitat utilisation species (Cambray 1990, 1994, 2004), the interaction The relative abundance of P. afer and S. capensis in each between the aggressive and territorial S. capensis and the microhabitat of each pool was estimated using five GoPro placid and schooling P. afer has not been explored. The Hero 3+ (GoPro Inc., USA) action cameras, in waterproof hypotheses for this work were 1) there is no difference in housings mounted on tripods; one covering each of the microhabitat occupancy for each of the species; 2) there selected microhabitats: inflow, outflow, deep open, woody is no difference in microhabitat occupancy between the debris, and fern-root wads. Cameras were set to take two species; and 3) there is no change in the microhabitat photographs (12-megapixel resolution), every five seconds occupancy of the two species following the introduction of to battery extinction, approximately 1.5 m away from each an artificial microhabitat. These hypotheses were evaluated microhabitat such that non-overlapping fields of view were by first establishing a baseline habitat occupancy for each ensured. Photographs were used in preference to videos of the two species (Hypothesis 1); compare the habitat in order to reduce the data-processing time (Hannweg occupancies of the two species (Hypothesis 2); and after et al. 2020). Photographs were viewed using Windows introducing an artificial habitat into the pools, assess the Photo Viewer (Microsoft Inc.) and relative abundance was change in habitat occupancy over a four-month period for estimated using MaxN following Cappo et al. (2003); the each of the species (Hypothesis 3). maximum number of P. afer, or S. capensis, individuals viewed in each photograph. The first 36 photographs were Methods discarded as acclimation time. Hannweg et al. (2020) showed that the MaxN population estimates of photographs Study species from five cameras in a pool were equivalent to population The Eastern Cape redfin, a small endemic cyprinid (max estimates from snorkel surveys. In this study, the sum of length ~110 mm) restricted to the headwaters of the MaxNs for each microhabitat was used as the population Baakens, Swartkops and Sundays rivers in the Eastern estimate for each pool. Cape (Chakona and Skelton 2017), is classified as Proportional occupancy, the proportion of the fish endangered in the 2017 IUCN Red List (Chakona et al. population in each habitat for each time segment (Rabeni 2017). The Cape Kurper is a small endemic anabantid (max and Sowa 1996), was used to compensate for the different length ~200 mm) restricted to the headwaters of the Cape sizes of each pool. The MaxN estimates for each species Fold Ecoregion from the Coega River, in the east, to the were not normally distributed (Shapiro–Wilk; p < 0.001), but Verlorenvlei River, in the west (Skelton 2001). Cape Kurper because of a large number of points in the datasets (750 was classified as data deficient in the 2017 IUCN-Red-List, proportional occupancies, for each microhabitat, in each because of unresolved with several genetically pool, for each species), ANOVAs were used (Van Hecke distinct lineages recognised throughout its distribution range 2012). To evaluate whether the proportional occupancies (Ellender et al. 2017; Chakona 2018; Bronaugh et al. 2020). of the respective species varied between the microhabitats (Hypothesis 1), two-way ANOVAs (factors: pool and habitat) Study area were performed for each species independently. Finding no The study was conducted from February to May 2017 significant results for pools, but significant results for habitat in the Fernkloof River, a perennial headwater tributary type and pool-habitat interaction, one-way ANOVAs of African Journal of Aquatic Science 2020: 1–9 3

habitat-type were performed for each species independently 30 cm PVC pipe to evaluate differences in proportional occupancy among Cable tie habitat types. Post hoc Tukey's Honest Significant 6 cm Difference tests (Tukey's HSD) were conducted to identify Chain statistical differences between habitat-type pairs. To Substrate evaluate whether the proportional occupancies of the two species varied between the microhabitats (Hypothesis 2), one-way ANOVAs for each habitat-type were performed to evaluate differences in proportional occupancy between the species. All data analyses were conducted using R 3.6.0 statistical software (R Development Core Team 2019), using p ≤ 0.05 to determine statistical significance. The Shapiro–Wilk test for normality was conducted using the shapiro.test function, one- and two-way ANOVAs using the aov function, and Tukey's HSD tests using the TukeyHSD function, all available in the R statistical software package.

Artificial habitat PVC pipes were chosen as an artificial substrate to provide an approximation to tightly packed woody debris and as a field comparison to the laboratory experiments of Kadye and Booth (2014). Artificial habitats were created from nine PVC pipes connected with cable ties (Figure 1). A Figure 1: Schematic diagram and photographs of artificial habitat chain was fed through the bottom pipes of each habitat and that was created out of 30 cm (length) by 6 cm (diameter) of PVC attached to 0.5 m lengths of 5 mm diameter threaded rods piping (large circles) attached together with cable ties (small circles) and weighed down with chains in the bottom row (arrows). Each driven into the substrate. An artificial habitat was placed in habitat was replicated four times and placed in four separate pools each of the four pools separate from the other habitats. within the Fernkloof tributary of the Swartkops River, Eastern Cape After a one-month acclimation period, four data-collection province, South Africa trips, approximately three weeks apart, were conducted to collect habitat occupation data and water physico-chemical parameters, as described for the baseline assessment. An Results additional camera was incorporated in each pool’s camera array to record the artificial habitat. To evaluate whether During the surveys, the turbidity of the water was very low the two species’ proportional occupancies within the (mean ± standard deviation: 0.34 ± 0.13 NTU), with an microhabitats changed after the introduction of the artificial average water temperature (19.5 ± 0.7 °C), a slightly acidic habitat (Hypothesis 3), one-way ANOVAs were performed pH (range: 4.32–5.64) and a conductivity of 232 ± 6 µs cm−1; for each habitat-type. Table 1 and Table S1 (Supplementary material). The substrate of the inflow and outflow of each pool mainly consisted of Multivariate analysis boulders (>256 mm), whereas within the pools the substrate The relationships between fish abundance (mean ranged from gravel (10–64 mm) to cobbles (64–256 mm) MaxN) and their habitats after the introduction of the with pockets of detritus and decaying plant material. The flow artificial substrate were explored further for both P. afer between pools was low throughout the study. and S. capensis, using a linear mixed effects model. Environmental variables (water depth, pH, conductivity and Baseline habitat utilisation temperature) were considered as predictors, however, pH Pseudobarbus afer appeared to prefer the deep open and and conductivity were subsequently excluded, because structured woody debris microhabitats within the pool, with they were constant over the four visits. To control for any a small portion preferring the structured fern root wads, and unknown effects unique to a pool or visit, visitation was very low occupancies in the shallow waters of the inflow nested within the pool as a random effect. In addition, the and outflow (Figure 2a). The two-way ANOVA returned no abundance (mean MaxN) of the other species was included significant difference in proportional occupancy between to evaluate whether the presence of one species influenced pools (F = 0.00, df = 3, p = 1), but a significant difference the density of the other species. A linear mixed effects model between the microhabitats (F = 18 756, df = 4, p < 0.001) was constructed for each species using the lmer function and the interaction term between pool and microhabitats in the R package lme4 (Bates et al. 2015) and ANOVAs (F = 99.9, df = 12, p < 0.001). The post hoc Tukey's HSD were performed on the linear mixed effects models using test showed that all pairwise microhabitat comparisons were the ANOVA function in the car package (Fox and Weisberg significant (All p < 0.001; Figure 2a). 2010) to identify the environmental variables that were Sandelia capensis appeared to favour structured woody significant in determining the abundance of the respective debris over the deep open and structured fern-root wad species. The ANOVAs were conducted using a type II Wald microhabitats and were absent from the shallow waters of the F-tests with a Kenward–Roger distribution factor, in order to inflow and outflow (Figure 2b). The two-way ANOVA returned reduce Type I errors (Kenward and Roger 1997). no significant difference in proportional occupancy between 4 Hannweg, Marr, Bloy and Weyl

Table 1: Summary statistics produced from habitat measurements in the four pools found in the Fernkloof tributary in the Eastern Cape, South Africa. Physico-chemical properties are shown as the mean value per pool ± SD (n = 3)

Mean Mean Water Length Volume Conductivity Turbidity Pool Location width depth temperature pH (m) (m³) (µs cm−1) (NTU) (m) (m) (°C) 1 33°43′24.64′′ S, 13 ± 0.4 2.6 ± 0.4 0.29 ± 0.02 4.52 19.5 ± 0.3 227 ± 1 0.52 ± 0.14 4.66 ± 0.35 25°17′7.80′′ E 2 33°43′26.65′′ S, 17 ± 0.5 3.0 ± 0.4 0.27 ± 0.02 7.25 18.8 ± 0.3 227 ± 1 0.24 ± 0.27 4.95 ± 0.15 25°17′5.28′′ E 3 33°43′27.26′′ S, 10 ± 0.3 3.5 ± 0.9 0.23 ± 0.01 4.37 19.7 ± 0.4 234 ± 1 0.30 ± 0. 02 5.49 ± 0.24 25°17′3.72′′ E 4 33°43′27.45′′ S, 10 ± 0.3 3.1 ± 0.7 0.47 ± 0.03 6.30 20.2 ± 0.7 240 ± 1 0.31 ± 0.02 4.87 ± 0.50 25°17′3.33′′ E

0.8 (a) Pseudobarbus afer

c 0.6 b

0.4

d

0.2 a e

0.8 (b) Sandelia capensis b TION OF POPULATION

0.6 c c PROPO R

0.4

0.2 a

a 0.0

Inflow Woody debris Deep open Fern root Outflow

HABITAT

Figure 2: Proportional occupancy for (a) Pseudobarbus afer and (b) Sandelia capensis in five habitat types within four pools of the Fernkloof headwater tributary of the Swartkops River, Eastern Cape, South Africa. Lower case letters indicate significant differences in the proportional occupancies between habitats (a common letter indicates no significant difference between habitats) pools (F = 0.00, df = 3, p = 1), but significant differences When comparing the habitat occupancy between the P. afer between the microhabitats (F = 13 721, df = 4, p < 0.001) and S. capensis (Hypothesis 2), a two-way ANOVA returned and the interaction term between pool and microhabitats no significant difference in proportional occupancy between (F = 261, df = 12, p < 0.001). The post hoc Tukey's HSD species (F = 0.00, df = 1, p = 1), but significant differences test showed that pair-wise microhabitat comparisons were all between the microhabitats (F = 14 781, df = 4, p < 0.001) and significant (p < 0.001) with the exceptions of those between the interaction term between species and microhabitats (F = the inflow and outflow (p = 0.992) and the deep open and 1 419, df = 4, p < 0.001). One-way ANOVAs were, therefore, fern-root wad microhabitats (p = 0.093); see Figure 2b. performed between species for each of the microhabitats. African Journal of Aquatic Science 2020: 1–9 5

All one-way ANOVAs returned significant results (p < 0.001) for P. afer to those following the introduction of the artificial across the microhabitats, confirming that each species habitat for each microhabitat independently (Hypothesis 3). occupied each habitat to different extents. The ANOVAs returned significant results for all microhabitats (p < 0.001) with the exception of the outflow (p = 0.786). Artificial habitat Unlike P. afer, the introduction of the artificial habitat Kadye and Booth (2014) found that under laboratory appeared to exert a major impact on the proportional conditions P. afer preferred artificial grass and pipe habitats, occupancy of the respective microhabitats utilised by while avoiding open water habitats. Following the introduction S. capensis. Noticeable decreases in the proportional of the artificial habitat, the majority of P. afer still appeared occupancies for the woody debris and fern-root wads to prefer the deep open and woody debris microhabitats, microhabitats were evident. The majority of the S. capensis although decreases in the proportional occupancies for now appeared to prefer the deep open and artificial habitats, these microhabitats were evident. A small portion preferred although the species still avoided the shallow inflow and the fern-root wads, whereas there were low occupancies in outflow habitats (Figure 3b). The two-way ANOVA between the inflow and outflow (Figure 3a). The occupancy for the pools and visits post artificial habitat introduction showed no artificial habitat was, however, higher than both the inflow significant difference in proportional occupancy between the and the outflow occupancies. The two-way ANOVA between factors or the interaction between the factors (F = 0.00, p = pools and visits post artificial habitat introduction reported no 1 for all). A one-way ANOVA for the proportional occupancy significant differences (F = 0.00, p = 1 for both). A one-way of S. capensis between microhabitats returned a significant ANOVA between microhabitats returned a significant result result (F = 2 238, df = 5, p < 0.001). A post hoc Tukey's HSD (F = 4 626, df = 5, p < 0.001). A post hoc Tukey's HSD test test of the proportional occupancy per microhabitat showed showed that all pair-wise microhabitat comparisons were that pairwise microhabitat comparisons were significantly significant for P. afer (p < 0.001) with the exception of that different for S. capensis (p < 0.001), with the exceptions of between the inflow and outflow (p = 0.054); see Figure 3a. those between the inflow and outflow (p = 1), between woody The impact of the introduction of the artificial habitat was debris and fern-root wads (p = 0.951), and between the deep evaluated by comparing the baseline proportional occupancy open and the artificial habitat (p = 0.058); see Figure 3b.

(a) Pseudobarbus afer 0.8

b 0.6 c

0.4 d e a a 0.2

0.8 (b) Sandelia capensis TION OF POPULATION

0.6 b c c

PROPO R b

0.4

0.2

a a 0.0 Inflow Woody debris Deep open Fern root Outflow Artificial

HABITAT

Figure 3: Proportional occupancy for (a) Pseudobarbus afer and (b) Sandelia capensis within four pools of the Fernkloof headwater tributary of the Swartkops River, Eastern Cape, South Africa, following the introductions of an artificial habitat. Lower case letters indicate significant differences in the proportional occupancies between habitats (a common letter indicates no significant difference between habitats) 6 Hannweg, Marr, Bloy and Weyl

The impact of the introduction of the artificial habitat was The higher proportional occupancies of S. capensis in evaluated by comparing the baseline proportional occupancy the structured woody debris and fern-root wad habitats of S. capensis to that following the introduction of the artificial could confirm the species’ preference for structure and habitat for each microhabitat independently (Hypothesis 3). cover over open water, e.g. Ellender et al. (2011). Being The ANOVAs returned significant results for all microhabitats a cryptic and structure-orientated species, S. capensis (p < 0.001) with the exception of the inflow (p = 1) and the favours microhabitats that provide refuge and where they deep open microhabitats (p = 0.030). are targeted less by aquatic and terrestrial predators (Swartz and Impson 2007). Sandelia capensis is an ambush predator Multivariate analysis feeding on insects, other invertebrates and small fish The multivariate analysis to identify the environmental (de Moor and Bruton 1988; Skelton 2001). The refuge offered variables that were significant in determining the abundance by these more complex structured microhabitats could aid in of the respective species demonstrated that microhabitat, increasing S. capensis’ predatory success on smaller fish. water temperature and the abundance of S. capensis were This increases juvenile S. capensis’ predator avoidance all significant for the abundance of P. afer (Table 2). For (Marriott 1998; Impson et al. 2007) and results in increased S. capensis, microhabitat and the abundance of P. afer population densities in such habitats, as observed in the were significant. The abundance of P. afer was positively palmiet Prionium serratum dominated habitats of the Twee associated with water temperature and the abundance of River (Marr et al. 2009). S. capensis, whereas the abundance of S. capensis was positively associated with the abundance of P. afer. Depth Artificial habitat was found to have a significant relationship with microhabitat Kadye and Booth (2014) found in laboratory conditions that type (ANOVA; F = 14.18, p < 0.001), which may explain why P. afer preferred grass and pipe habitats, while avoiding depth was not significant for either species. open water habitats. However, in this study, P. afer favoured the deep open habitat over the other four habitats. The Discussion laboratory setting of the experiment conducted by Kadye and Booth (2014) may have unsettled the P. afer and Pseudobarbus afer and S. capensis appear to prefer deeper resulted in them hiding. The introduction of the artificial and structured habitats, while avoiding the shallow, faster habitat reduced the proportional occupancy of P. afer in all flowing water of the inflows and outflows of the pools, the natural microhabitats, except the outflow. In natural S. capensis more so than P. afer. The reason might be the surroundings, P. afer were not observed using the artificial faster flowing water of the inflow microhabitat is energetically habitat (PVC pipes) as a refuge, but were observed feeding more demanding for fish to forage in (e.g. Facey and on the material that had settled on the artificial habitat. As Grossman 1990), or because the shallow nature of the inflow seen in the baseline study, P. afer favoured the deep open and outflow habitats may also increase the predation risk microhabitat over the other habitats available in the pool, from diving or wading fish-eating birds (Kadye and Booth although they had higher proportional occupancies for the 2014), kingfishers and herons, respectively. artificial habitat than for the inflow and outflows of the pools. Pseudobarbus afer and S. capensis were found to coexist Sandelia capensis, an aggressive and territorial, structure in three of the five microhabitats (woody debris, fern-root orientated species (Cambray 1990), rapidly colonised the wads, and deep open), although P. afer were approximately artificial habitats and may have outcompeted P. afer for these seven times more abundant than S. capensis in these habitats, thereby reducing P. afer utilisation to foraging on microhabitats. Pseudobarbus afer were most abundant in the surface of the artificial habitat. The artificial structures the deep open and woody debris microhabitats, whereas provided refugia for S. capensis and this species was S. capensis were recorded relatively few times in open observed resting within the pipes and actively moving from habitats. Pseudobarbus afer exhibited schooling both within pipe to pipe. The introduction of the artificial habitat resulted and outside of structured habitats during the middle of the in a significant shift in relative microhabitat occupancy by day when the observations were made, especially in the S. capensis in all microhabitats with the exception of the deep open habitat, observations consistent with Ellender et fast, shallow waters of the inflow. It is likely that S. capensis al. (2018). As a result of the midday timing of the recordings, colonised the artificial habitat, because the pools in the the assertion of strong diurnal activity made by Kadye and Fernkloof River have limited microhabitats available. The Booth (2014) could not be evaluated. fern-root wads are on rock faces on one bank of the pool

Table 2: Results from an ANOVA using linear mixed effects models for the Pseudobarbus afer and Sandelia capensis MaxN. Bold indicates statistical significance

Species Habitat Temperature Depth Other species AIC S. capensis F = 18.466 F = 3.832 F = 0.038 F = 5.318 90.9 p < 0.001 p = 0.058 p = 0.847 p = 0.025

P. afer F = 28.198 F = 6.993 F = 0.012 F = 4.916 210.5 p < 0.001 p = 0.026 p = 0.913 p = 0.031 African Journal of Aquatic Science 2020: 1–9 7 and they do not extend much into the pools, and the woody Tourism permit numbers CRO 37/17CR and CRO 38/17CR. Any debris constitutes less than 10% of the pool habitat. opinion, finding and conclusion or recommendation expressed in this The abundance of both species was positively associated material is that of the author(s) and the NRF and Rhodes University do with the abundance of the other species. This was not accept any liability in this regard. unexpected, because of the aggressive and territorial nature of S. capensis and that S. capensis is an ambush predator ORCIDs of small fish, including Pseudobarbus species (Skelton 2001). Alternatively, the overlap in the habitat preferences SM Marr https://orcid.org/0000-0001-8655-5522 of the two species and the habitats available could be a OLF Weyl https://orcid.org/0000-0002-8935-3296 plausible explanation. References Conservation value of the artificial habitat Habitat complexity strongly affects the structure and dynamics Abell R, Thieme ML, Revenga C, Bryer M, Kottelat M, Bogutskaya of ecological communities, with increased complexity often N, Coad B, Mandrak N, Contreras-Balderas S, Bussing W, leading to greater species diversity and abundance (Smith et et al. 2008. Freshwater Ecoregions of the world: a new map of al. 2014). Habitat degradation results in the simplification of biogeographic units for freshwater biodiversity conservation. BioScience 58: 403–414. habitat complexity that can result in declines in native species Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed (Didham et al. 2007; Hermoso et al. 2011). Artificial habitats effects models using lme4. Journal of Statistical Software 67: 1–48. can be used as freshwater fish conservation measures Bronaugh WM, Swartz ER, Sidlauskas B. 2019. Between an (Schlaepfer et al. 2005; Yokomizo et al. 2007; Westhoff et ocean and a high place: Coastal drainage isolation generates al. 2013) to boost population numbers by providing habitats endemic cryptic species in the Cape kurper Sandelia capensis critical to fish species. In this study, the outcome of the (: Anabantidae), Cape Region, South Africa. introduction of artificial habitat was the colonisation of the Journal of Fish Biology 96: 1087–1099. artificial habitat by the more widespread, and putatively less Cambray JA. 1990. Early ontogeny and notes on breeding threatened of the two native species, S. capensis. Although behaviour, habitat preference and conservation of the Cape the PVC pipes used as an artificial habitat may not promote kurper, Sandelia capensis (Pisces: Anabantidae). Annals of the Cape Provincial Museums: Natural History 18: 159–182. the conservation of the endangered P. afer, this study has Cambray JA. 1994. The comparative reproductive styles of two shown that artificial habitat placement may benefit populations closely related African minnows (Pseudobarbus afer and P. asper) of S. capensis that are declining, especially following habitat inhabiting two different sections of the Gamtoos River system. degradation. The PVC pipe based artificial habitat is not Environmental Biology of 41: 247–268. optimal for P. afer and alternative artificial habitat designs Cambray JA. 2004. Spawning behaviour of Sandelia capensis should be explored to find the attributes of the artificial habitat (Teleostei: Anabantidae). Ichthyological Exploration of that would benefit P. afer without extensively expanding the Freshwaters 15: 311–322. habitat suitable for S. capensis. Cappo M, Harvey E, Malcom H, Speare P. 2003. 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An evaluation of artificial reef structures Nature Reserve for their assistance during the fieldwork. This study as tools for marine habitat rehabilitation in the Maldives. Aquatic was financially supported by the National Research Foundation Conservation 9: 5–21. (NRF) - South African Research Chairs Initiative of the Department of Darwall W, Bremerich V, De Wever A, Dell AI, Freyhof J, Gessner Science and Innovation (DSI) (Grant No. 110507), Water Research MO, Grossart HP, Harrison I, Irvine K, Jähnig SC, et al. 2018. Commission of South Africa (K5/2538), the NRF Professional The Alliance for Freshwater Life: A global call to unite efforts Development Programme (Grant No. 1010140), the Deutscher for freshwater biodiversity science and conservation. Aquatic Akademischer Austauschdienst (DAAD) and the DSI/NRF Centre Conservation: Marine and Freshwater Ecosystems 28: 1015–1022. of Excellence in Invasion Biology. We acknowledge the funding de Moor IJ, Bruton MN. 1988. 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Manuscript received: 31 May 2019, revised: 12 December 2019, accepted: 16 January 2020 Associate Editor: A Chakona