CSIRO PUBLISHING
Wildlife Research, 2010, 37, 240–248
www.publish.csiro.au/journals/wr
Detecting, but not affecting, nest-box occupancy Tracey Moore A,C, Paul de Tores B and Patricia A. Fleming A A
School of Veterinary and Biomedical Science, Murdoch University, South Street, Perth, WA 6150, Australia. B Department of Environment and Conservation, Wildlife Research Centre, PO Box 51, Wanneroo, WA 6946, Australia. C Corresponding author. Email:
[email protected]
Abstract Context. Nest boxes are a useful tool in the reintroduction, conservation and monitoring of many hollow-using species. Aims. All forms of nest-box monitoring involve some form of invasion, often upsetting their continued use by occupants. We conducted a pilot study to investigate and validate the innovative use of temperature dataloggers (iButtons®) to remotely monitor nest-box use, leaving the nest-box occupants untouched. Methods. In captivity, iButton recordings revealed the duration and time of day when each of the three nest-box designs was occupied by Pseudocheirus occidentalis (western ringtail possums); the accuracy of occupancy data was validated by unobtrusive infrared video recording. In the field, where translocated P. occidentalis and naturally occurring Trichosurus vulpecula (common brushtail possum) populations are present, hair sampling at the nest-box entrances (in addition to iButton recording) was used to identify the mammal species present. Key results. Nest-box use by captive P. occidentalis validated iButtons as a useful remote-monitoring tool, with 200 individuals released between 1991 and 2006 (de Tores 2008, unpubl. data). At the time of the present study, four individuals were being monitored through radio-telemetry to assess the survivorship of P. occidentalis (J. Clarke, pers. comm.). Within the park, there is a naturally occurring population of a potential competitor for den sites, the common brushtail possum (Trichosurus vulpecula, Family Phalangeridae, body mass 2–3 kg) (de Tores et al. 2004; Nowicki 2007). Forty-eight nest boxes (16 of each of the three designs) were placed in trees (one of each design per tree) at Leschenault Peninsula Conservation Park. Nest-box use was monitored during 17 weeks from June to September 2007 (Austral winter, when daylength was ~10–11 h). Each nest box was equipped with two iButtons, one taped to the floor inside the box (Tin) and a second taped directly on top of the nest box (Tout). Each pair of iButtons logged simultaneously every 20 min. Possum presence was categorised post hoc into ‘shortterm occupancy’ and ‘residence’ on the basis of the iButton data. Short-term occupancy of a nest box was defined as Tin – Tout 2 s.d. C for less than 2 h, whereas residency was defined as Tin – Tout 2 s.d. C for more than 10 h (usually Fig. 1. Three nest-box designs were tested in the study. (a) An artificial drey (nest) was constructed with two hemispherical hanging baskets wired together, with an entrance aperture cut into one side. Foliage from Agonis flexuosa was woven through the wire to mimic a drey. (b) A hexagonal medium-density fibreboard box with two entrances and (c) a rectangular pine box with a single entrance. We acknowledge the input of numerous stakeholders in designing these boxes.
Detecting, but not affecting, nest-box occupancy
Thermal properties of the nest-box designs Experiments to identify the thermal properties of each nest-box design were carried out in a temperature-controlled room at Murdoch University. Each nest box was provided with an internal heat source during these trials, namely an aluminium foil-wrapped 15-W lamp. Each nest-box design had an internal (Tin) and external (Tout) iButton attached as per field trials, and room temperature was recorded with a third iButton. Trials were carried out where the room was cooled (from ~25C to 5C) over the space of ~4 h to monitor the nest-box cooling rate, or was heated (from ~5C to 25C) over ~4 h to monitor the nest-box heating rate.
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between 0600 hours and 1800 hours during diurnal resting or denning for these nocturnal species). During the field trial, there was no record of nest-box occupancy (Tin – Tout 2 s.d. C) between the 2- and 10-h durations. In addition to monitoring with iButtons, each nest box was physically checked weekly for occupancy. Additionally, doublesided tape (Selleys Chemical Co., NSW, Australia) was applied to the entrance of each nest box to collect hair from animals as they entered the nest box. Tape was checked during the weekly physical nest-box inspection and replaced if defective (i.e. owing to water damage). Hair was collected and removed from the tape with a citrus-based stain remover (to minimise damage to the shaft) before it was mounted in glycerol and identified microscopically. Identification was based on differences in the medulla pattern of the shield region of primary guard hairs (Brunner et al. 2002).
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Under captive and field situations, iButtons reliably identified the occupancy of nest boxes. Positive deviation from the line of equity (Tin = Tout) coincided with the occupancy of nest boxes. For example, Fig. 2a demonstrates the temperatures recorded for a rectangular nest box in the field. The following three distinct clusters/clouds of data points are discernable: (i) Data points representing a linear/near linear relationship between Tin and Tout where (Tin – Tout) was 3C (average 6.73 2.50C). These data were interpreted as indicating occupancy by a possum and, on at least two occasions, this corresponded with a physical presence of an animal during a weekly nest-box check. Although the average thermal difference (Tin – Tout) varied with the absolute ambient temperature, Tin was maintained at a high value (averaged 22.33 4.27C for data shown in Fig. 2a). (iii) A less tightly grouped cluster of data points where Tin < Tout. This occurred when solar radiation heated the external iButton only. This interference reoccurred at the same time of day during consecutive days (Fig. 2b).
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Fig. 2. Example of raw iButton data used to determine nest-box use for an occupied rectangular nest box placed at Leschenault Peninsula. Each iButton logged every 20 min for 17 weeks. (a) Each point indicates a simultaneous record of temperature by an iButton taped internally to the nest-box floor (Tin) and an iButton taped to the top of the nest box (Tout). Occupancy is indicated as a positive difference (Tin – Tout) of >4C (2 the s.d. value of this difference), as shown by the dotted line. When the sun directly hit the nest box, Tout was higher than Tin, termed sun interference (the sun hit this particular nest box between 1330 hours and 1430 hours almost every afternoon). Similar external and internal temperatures (Tin – Tout < 4C) were taken to indicate no nest-box occupant, termed no activity. A few data points where Tin – Tout < 4C occurred in the middle of the day during the middle of an occupancy event. During this time, Tin did not change markedly over time, whereas Tout rose (predicted because of sun interference). From the nocturnal behaviour of these animals and similar interference at the same time of day on successive days, possum presence could be reliably inferred and these data are therefore indicated as positive for possum presence. (b) Temperature within (Tin) and outside (Tout) this nest box over 2 days demonstrates sun interference (each afternoon), and animal presence over 1 day. Note the sharp increase in the temperature with animal presence and the slow incline (but sharp peak) in temperature when solar radiation warms the nest box.
After viewing graphical presentation of these data, a difference of 2 s.d. (1.96C) was investigated as a suitable cut-off for distinguishing occupancy of these next boxes
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(i.e. (Tin – Tout) > 4C indicated nest-box occupancy for the field trials). The use of this factor of the standard deviation of the temperature differences as a cut-off through captive trials was investigated, as detailed below. Captive trials During captive trials, where ambient temperatures (10.9 3.4C) were lower and more stable than the field recordings (13.8 4.5C), a recorded difference (Tin – Tout) of >2C (i.e. 2 the s.d. value of 0.91C) could reasonably be inferred (validated by video recordings) to indicate the presence of a nest-box occupant. This cut-off minimised both false positive and false negatives recordings (these data were calculated with cut-offs of both 3C and 4C, for comparison). A difference of >2C confirmed occupancy of the artificial drey on 95.4% of occasions (Table 1). Of the erroneous data, 82.0% occurred at the beginning or end of an occupancy event and may be interpreted as a result of a lag in warming up or cooling down of the iButton. For the drey, the number of false positives (2.9% of records) was close to the number of false negatives (1.8% of all records). The remaining 18.0% of erroneous data (a total of 0.8% of all data logged) were negative iButton data (the temperature logger failed to record the presence of the possum) during the middle of an occupancy event, presumably because the animal had shifted its position and was no longer in direct contact with the temperature logger or because Tout had risen similarly. A slightly greater error was observed for the hexagonal nest-box design, with 94.1% of iButton records correctly reflecting the nest-box occupancy (Table 1). False positives accounted for 2.6% of all data records, and false negatives for 3.3%. Of the erroneous data, 45% occurred at the beginning or end of an occupancy event, 25% reflected the nest-box warming >2C compared with the ambient temperature in the absence of an occupant, 19.5% were negative data during the middle of an occupancy (i.e. because of shifted position) and 10.4% were due to a failure to warm the iButton during a short (~40 min) occupancy event, before the possum vacated the nest box. Table 1. Occupancy of the three nest-box designs (artificial drey, hexagonal nest box and rectangular nest box) as indicated by iButtons® and infrared video recording Each value is the number of 10-min recording intervals; the trial ran over a period of 9 days and 3 h iButton® data
Artificial drey Possum presence Possum absence Hexagonal Possum presence Possum absence Rectangular Possum presence Possum absence
Video recording Possum Possum presence absence 734 38
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Pseudocheirus occidentalis demonstrated individual preferences for different nest-box designs (Fig. 4). For example, the male in the enclosure monitored via infrared camera did not use the rectangular nest box at all during the period (9 days, 3 h) of video monitoring. Therefore, we were unable to validate occupancy inferred by iButton data for the rectangular nest-box design. However, the iButton data correctly reflected the absence of this possum for 98.7% of records (Table 1). Of the 1.3% of (false positive) errors, all occurred at the same time of day and more than half occurred at the same time as the same error was recorded for the hexagonal design; presumably, these data reflect the boxes warming slightly in response to solar radiation. An additional type of error was evident close to dusk, when the rapid cooling of the iButton measuring ambient temperature was not reflected by a comparable rapid cooling of iButtons located within the nest boxes. As a consequence of this discrepancy, 2.01% of the 10 338 time points recorded two or all three nest boxes simultaneously occupied; 77% of these errors occurred between 1500 hours and 1900 hours. Ambient temperature had fallen an average of 0.30 0.37C over the half hour preceding these erroneous time points. This type of error can be visualised in Fig. 2b, where Tout heated up quicker than Tin towards the afternoon of Day 2 (no possums present), but also cooled down quicker than Tin after the sun had moved past this nest box. For the captive trials, iButtons logged temperature every 10 min and the nest-box preference could be inferred as the percentage of time each nest box was occupied. Overall, all nest-box designs were used (Figs 3, 4) during the captive trials, with 256 nest-box use events recorded, with the period of occupancy ranging from 10 min to 13 h. Occupancy was largely determined by an individual preference for the nestbox design, with one possum never entering the artificial drey (Fig. 3a). Nest-box use appeared to be associated with time of day and weather patterns (Figs 3, 4). Possums were more likely to remain in nest boxes during the day, when they spent an average of 86% of their time inside one of the nest boxes, compared with only 29% overnight (Fig. 4a). Warmer temperatures were experienced during the day, and therefore greater occupancy was recorded for warmer ambient temperatures. Notably, however, a drop in the nest-box use was recorded for temperatures >17C (Fig. 4b). There was a slight increase in the use of all nest boxes with increasing rainfall (Fig. 4c). Nest-box occupancy at field sites We recorded a low incidence of nest-box use by the resident and translocated possums at Leschenault Peninsula Conservation Park (determined via direct weekly observations, iButton data and hair samples taken from the entrances of the nest boxes). During the 16–17 weeks of surveying, we recorded a total of 34 hair samples, identified as P. occidentalis (n = 7) and T. vulpecula (n = 27) (Table 2). Fourteen hair samples were associated with iButton temperature data indicating the presence of a warm body in the nest box for some period during the week the hair was deposited. However, 20 samples were collected from nest boxes that showed no indication of
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continued warming (i.e. iButton data: Tin – Tout < 2 s.d. C ) and were, therefore, interpreted as ‘investigations’, not occupancy. iButton data indicated that there were 13 short-term occupancies (during which time the temperature inside the nest box rose, with Tin – Tout > 2 s.d. C over a period of 2 s.d. C over a period of 10 h). Hair samples and weekly physical checks confirmed the occupant as T. vulpecula. This nest box was occupied a total of 11 days, and was more commonly used on cooler, dry days (Table 2). None of the dreys or hexagonal boxes was occupied for 10 h during the monitoring period of the present study (although see below). Our data suggested that P. occidentalis investigated but did not reside in any of the 48 nest boxes during the length of the study. However, subsequent radio-tracking of these translocated animals by another researcher did record residency within a rectangular (2 nights) and a hexagonal (2 nights) nest box by two individuals (J. Clarke, unpubl. data) during late spring. Because of the low number of study animals, we would not like to infer on the nest-box preferences of the species and how the weather might affect these choices, only to point out that such comparison is possible.
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Thermal properties of each nest-box design When the three nest boxes were allowed to thermally equilibrate in either a cool (5C) or warm (25C) room, in the presence of an internal heat source (a lamp placed in each nest box), the rectangular nest box maintained a higher temperature (average ~5C > Ta), followed by the hexagonal nest box, whereas the artificial drey retained the least heat (was cooler under both conditions than the other two nest-box designs). The hexagonal box also retained the most heat when the room was cooled from 25C to 5C (i.e. showed the slowest cooling rate). All nest boxes heated up at a similar rate. The averaged cooling time from ~37C measured for five iButtons can be expressed as Temperature (C) = 37 – 1.93 Ln (mins). Under these experimental conditions, it takes an iButton only ~3 min to cool from 37C to 35C and ~35 min to cool from 37C to 30C at an Ta of 24C. Cooling time would therefore be dependent on the temperature the iButtons attained as well as the current Ta. Presumably, warming times will depend on the
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Fig. 3. Occupancy of the three nest-box designs (artificial drey, hexagonal and rectangular nest boxes) by (a–c) three individual western ringtail possums (Pseudocheirus occidentalis); data are shown according to days of different levels of rainfall. Animal c was also monitored by video camera. Animals were held individually at the Dwellingup Research Centre for a total of 26 days, of which, no rainfall was recorded for 4 days, light rainfall (10 mm per 24 h) over 8 days. Rainfall was recorded daily at 0900 hours for the preceding 24 h by the Bureau of Meteorology in Dwellingup.
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temperature and heat loss from the body part of the animal in contact with the temperature logger. Warming of the next box by either solar radiation or an animal body is demonstrated graphically in Fig. 2b. This figure demonstrates that warming the nest box by solar radiation increases temperature (Tout and to a lesser extent Tin) incrementally, whereas the warmth from an animal body sharply raises the temperatures recorded by the internal iButton (Tin).
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Although some attempt was made to ascertain nest-box design preferences in the present study, the three P. occidentalis individuals used in the captive trials demonstrated very different preferences in terms of nest-box use (Fig. 3). In principle, however, the nest-box preference could have been inferred as the percentage of time each nest box was occupied, if more study animals had been available.
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We have demonstrated that a simple thermal principle can be effectively used to monitor occupancy of nest boxes. iButtons® are small, rugged, stand-alone temperature loggers that may be deployed in field settings to indicate nest-box occupancy by endothermic homeotherms. The majority of published studies using iButtons record skin and core-body temperatures. A few studies have used iButtons to examine the thermal properties of nest boxes or nesting sites (Wiebe 2001; Duckworth 2006; Garcia-Navas et al. 2008; Isaac et al. 2008) or the onset of incubation and timing of nest failure for large birds (Badyaev et al. 2003; Cooper et al. 2005; Hartman and Oring 2006). The present study is one of the first to utilise iButtons to monitor nest-box occupancy and preferences, and here we have validated the use of simultaneous recordings (inside and outside nest boxes) to detect even short-duration occupancy events. Most published studies examining nest-box occupancy have been limited to physical checks for occupants (e.g. Ward 2000; Lindenmayer et al. 2003). By contrast, the use of temperature loggers such as iButtons leaves the nest-box occupant(s) undisturbed. Combining the use of iButtons with regular collection of hair samples enables identification of those species that have occupied the nest box. The major advantage of iButtons is that they tell an investigator not only if a nest box was occupied, but also for how long the occupancy lasted and when it occurred. Data obtained may therefore be used to assess the preference for different nest-box construction, placement, orientation and other variables, with the potential to influence nest-box use. Furthermore, the comparison of temporal recordings with environmental conditions such as time of day (day/night), temperature and rainfall enables examination of nest-box occupancy under different weather conditions, which
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Fig. 4. In addition to individual differences in the preference and use (Fig. 3) of the three nest-box designs, nest-box occupancy was affected (a) by the time of day, (b) ambient temperature and (c) rainfall. (a) Occupancy was greatest for daylight hours in these nocturnal animals, during which time, higher temperatures were recorded. (b) Nest-box use dropped off for temperatures over 17C, and (c) increased on rainy days (rainfall categories as per Fig. 3).
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Table 2. Incidence of short-term occupancy (for 17C suggests that nest-box occupancy may become uncomfortable for them during these warmer periods. However, we advise a cautious interpretation of our findings, because the captive data were collected over a limited period (26 days), within only one season (winter). Although we recorded 256 nest-box occupancy events for captive animals, these events were for only three individuals and we therefore have to be cautious in respect to interpretation of nest-box preferences by these animals. For our very different nest-box designs, iButtons correctly indicated nest-box occupancy over 94% of the time. Excluding errors owing to warming up or cooling down (at the beginning or end of an occupancy event, respectively), which were reasonably similar in terms of frequency, the above value may be as high as 98.2%. We investigated the thermal properties of our three nest-box designs and found that the rectangular box (with a single entrance) retained heat and cooled slower than the hexagonal box (with two entrances), whereas the dreys retained least heat of all. We predicted that there may have been differences in the efficacy of iButton data as an indicator of occupancy for the three nest-box designs, given that they had different thermal properties; however, our data indicated that a cut off of (Tin – Tout) >2 s.d. C was appropriate for each design we tested. We recommend that future researchers investigate the thermal properties of their nest-box designs or tree hollows to enable accurate interpretation of similar iButton data. Furthermore, climatic differences will influence the choice of the appropriate cut-off, because we noted greater variability in (Tin – Tout) for higher than for low temperatures. Future studies may also need to consider the thermal properties of the nest box being used, in terms of the placement of the internal and external temperature loggers. Adults of the two species included in the study weigh from 0.8 kg to 4.5 kg (Menkhorst and Knight 2004). It is possible that smaller species may not generate sufficient heat to enable accurate interpretation of occupancy from thermal properties, or the animal may move out of contact with an iButton taped
to the floor centre of nest boxes as large as those used in the present study. Nest-box design may prevent this issue, if smaller nest boxes (with a reduced floor area) are designed for smaller species, or perhaps multiple iButtons could be considered, both of these increasing the chances of an animal resting on the internal iButton. Finally, we cannot predict the accuracy of thermal readings for occupancy by species that utilise torpor, and this would require further investigation. We tested the use of iButtons during the Austral winter when ambient temperatures ranged from a minimum of 3.6C to a maximum of 22C. It is possible that higher ambient summer temperatures may require a different threshold for the temperature difference (Tin – Tout), although we believe the principle of a warmer interior reflecting the presence of a warm body could also be used to infer occupancy during hotter months. The issue of solar radiation confounding analysis is easily overcome during data analysis; however, it should also be considered when nest boxes are being placed in the field. Potentially, a sun shield could be considered if nest boxes are likely to encounter intense solar radiation. On a final note, the present study was initiated to investigate the potential role of nest boxes in the conservation of P. occidentalis. We note that, because of individual differences, such a study requires greater numbers of animals than were able to be included in the present study, and requires the tracking of animals over extended periods, and if possible, over all seasons of the year. We conclude that iButtons are a valuable tool for determining nest-box occupancy and preference with very little error. Furthermore, Cawthen et al. (2009), by using a similar method to the one used in the present study, indicated that iButtons may have the potential to monitor tree hollows as well as nest-box use. We believe that nest-box occupancy can be unobtrusively monitored via iButtons during wildlife translocation or as a part of investigations into habitat enrichment by supplying nest boxes. Acknowledgements Thanks go to John Gunnell, Matthew Moore, Kiri Clarke, Kanyana Rehabilitation Centre, Fauna Rehabilitation Foundation (FRF, now Native Animal Rescue, NAR), Fostering and Assistance for Wildlife Needing Aid (FAWNA), Uta Wicke and Bethwyn Hastie. We thank Sean Garretson and
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John Angus for technical support with cameras and hair identification, respectively, and Dave Beatty, Sabrina Trocini, Gillian Bryant, Todd McWhorter, Judy Clarke, Tom Robinson, Brian Smith, Ralph Staines, Rob Hill and Judy Turner for field support. Thanks go to Judy Clarke for access to unpublished data. We acknowledge the generous funding support from the Australian Veterinary Association Welfare trust.
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Manuscript received 20 August 2009, accepted 8 April 2010
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