*Article* **Riparian Bird Occupancy in a Mountain Watershed in the Colorado Mineral Belt Appears Resilient to Climate-Change-Driven Increases in Metals and Rare Earth Elements in Water and Aquatic Macroinvertebrates**

**Kelly E. Watson and Diane M. McKnight \***

Institute of Arctic and Alpine Research, University of Colorado, Boulder, CO 80303, USA **\*** Correspondence: diane.mcknight@colorado.edu

**Abstract:** Acid rock drainage (ARD) impacts species composition in mountain streams. The potential impact for riparian birds experiencing elevated metal uptake by consumption of benthic invertebrates is concerning but not well studied. We investigated the influence of metal and rare earth element (REE) content in benthic invertebrates on the presence of breeding birds in an ARD-impacted watershed in Colorado, USA, where tree swallows in nest boxes had previously been found to have elevated metal concentrations at some sites. The concentrations of particular REEs in invertebrates were higher than those for cadmium or lead. Avian point counts indicated that most bird species detected were present at most sites, and that tree swallows were rarely found. Occupancy models showed that the availability of shrub or forest habitat was a good predictor for a few habitat-specialists, but metal and REE concentrations in water and invertebrates were not good predictors of avian presence. For other species, neither habitat type nor water quality were important predictors. Overall, this study indicates that the climate-change-driven increases in metals and REEs may not influence the presence of riparian birds in ARD-impacted streams.

**Keywords:** acid mine drainage; riparian birds; rare earth elements; benthic invertebrates

### **1. Introduction**

Acidic drainage can occur naturally wherever geology puts sulfidic minerals in contact with air and water and is referred to as acid rock drainage (ARD). Major water quality concerns arise in regions where mining activities greatly accelerate this weathering process, which is referred to as acid mine drainage (AMD) [1]. In the late 1800s, during the Colorado Gold Rush, extensive hard-rock mining took place throughout the Colorado Mineral Belt in the Rocky Mountains (USA). Many mining claims were abandoned just as quickly as they were excavated and piles of waste rock or mine tailings are common throughout the Colorado Rocky Mountains to this day. The US Government Accountability Office has estimated that there are hundreds of thousands of abandoned mines scattered throughout the Western United States [2]. These abandoned mines continue to contribute acidic, metalenriched water to mountain streams, impairing the aquatic ecosystems and acting as a source of trace metals to drinking-water supplies [3]. Recent studies have found that rare earth elements (REEs) are also elevated in ARD-impacted streams in the Colorado Mineral Belt and that summertime concentrations of both metals and REEs are increasing due to climate change [4].

A pervasive impact of ARD streams is the reduction in species richness, occurring across microbial, algal, and invertebrate communities [5,6]. Genomics methods have shown that microbial taxa in ARD streams are dominated by specialized acidophile organisms [7,8]. Fish and amphibians are often absent due to metal or acid toxicity [9,10]. The drivers for ARD impacts are not only the acidity itself and metal toxicity but also the precipitation of

**Citation:** Watson, K.E.; McKnight, D.M. Riparian Bird Occupancy in a Mountain Watershed in the Colorado Mineral Belt Appears Resilient to Climate-Change-Driven Increases in Metals and Rare Earth Elements in Water and Aquatic Macroinvertebrates. *Diversity* **2023**, *15*, 712. https:// doi.org/10.3390/d15060712

Academic Editors: Lin Zhang, Jinniu Wang and Fabio Stoch

Received: 5 March 2023 Revised: 23 May 2023 Accepted: 24 May 2023 Published: 27 May 2023

**Copyright:** © 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

iron and aluminum oxides [11]. In streams with high amounts of metal oxide precipitates covering the streambed, benthic organisms such as primary producers, periphyton, and invertebrates can be smothered completely [12,13]. Ecosystem processes, such as litter decomposition, are also suppressed [14,15]. However, in streams with a low pH and high dissolved metal concentrations, but without precipitates, a few tolerant species of benthic invertebrates may be as abundant as in pristine streams. For example, McKnight and Feder [12] found no difference in the benthic invertebrate abundance in an ARD stream compared to a nearby pristine stream, and the community was dominated by the stonefly *Zapada haysii* which is common in ARD streams.

Benthic macroinvertebrates are often used as bioindicators of stream health, and studies of acidic drainages have shown that invertebrates accumulate metals in their bodies [16,17]. There are few studies of REE content in benthic invertebrates and no studies of REEs' accumulation in benthic invertebrates in ARD streams. In a study of temperate lakes in Canada, Amyot et al. [18] found that REE concentrations ranged from 0.1 to 1 ng/g and that REEs were subject to trophic dilution, with lower concentrations at higher trophic levels. The accumulation of metals and REEs in benthic invertebrates is of concern from an ecosystem perspective because of the potential for transport up the food web through bioaccumulation to fish and other predators [19,20].

There has been little investigation into whether elevated metal or REE concentrations in streams affect nearby terrestrial organisms. One potential pathway for these elements to enter terrestrial food chains is the emergence of aquatic insects that spend their larval stages in streams and can be consumed by birds as adult flying insects. Studies have shown that birds acquire elevated metals from prey in a variety of environments, including from aquatic sources [21–23]. Environmental acidification and the resulting increased mobility of metals, especially cadmium, mercury, and lead, has been a long-term concern for birds [24,25].

The few studies of ARD effects on terrestrial organisms have addressed concerns related to ingesting elevated levels of toxic metals such as lead (Pb) and cadmium (Cd), which may lead to a lower survival in breeding birds. There is some evidence for reduced density, delayed breeding, and fewer offspring produced by Eurasian dippers (*Cinclus cinclus*) and Louisiana waterthrushes (*Seiurus motacilla*) breeding along acidified streams in Wales and Pennsylvania, respectively [26,27]. The most acidic streams in the dipper and waterthrush studies had pH values of 4.5, which is higher than many ARD streams. In a study of tree swallows (*Tachycineta bicolor*) occupying nest boxes adjacent to ARD streams in the Snake River watershed in Colorado (USA), Custer et al. [28] found that at sites where invertebrates had elevated metal concentrations, nestlings also had elevated, but not toxic, Pb concentrations in liver tissue. It has not yet been determined whether ARD affects the behavior, survival, reproduction, or population dynamics of free-living avian species living adjacent to ARD streams. In a recent study of 35 first- and second-order stream ecosystems impacted by ARD in the Colorado Mineral Belt, Kraus et al. [29] found that adult aquatic invertebrates had lower contents of Cd and Pb than the larval stages living in the streams, reducing the impact of metal transfer to insectivorous riparian spiders. These lower metal contents could potentially also limit the impact of metal transfer to insectivorous riparian birds.

The present study was conducted in the same watershed as the study by Custer et al. [28] and assessed the potential impacts to all riparian birds in a large montane watershed with both pristine and metal-impacted sub-watersheds. The two objectives were to determine (i) both the trace metal and REE contents of benthic invertebrates in the watershed to obtain more complete information on ARD impacts, and (ii) whether birds breeding in riparian forests and wetlands in the watershed are less likely to occupy sites adjacent to the ARD-impacted streams compared to the pristine streams. Given that climate change is expected to continue to exacerbate the impacts of ARD [30], the results of this study help to establish the degree of impact of ARD on both aquatic and terrestrial wildlife.
