Tackling the tide: A rapid assessment protocol to detect terrestrial vertebrates in mangrove forests

Abstract

Globally, the occurrence of terrestrial vertebrates in mangrove forests is poorly documented, with little empirical data available. This knowledge gap is, at least in part, explained by the challenging survey conditions typically found in these environments. As an ecological understanding of ecosystems is essential to guide conservation management actions, a lack of baseline biodiversity surveys can leave ecosystems vulnerable to degradation. To address this, we developed and tested a rapid assessment protocol for tidal regions (RAPTR), that uses a range of techniques to detect mammals, reptiles and amphibians in mangrove habitat subject to daily tidal inundation. Our approach uses seven commonly used fauna detection techniques (live traps, camera traps, nocturnal transects, hair tubes, artificial terrestrial and arboreal refuges, and high-frequency acoustic monitoring). RAPTR was implemented over four consecutive nights at each of the 10 sites spanning temperate to tropical mangrove regions of Australia. We detected 65 species of terrestrial vertebrates, of which 42 species have not previously been reported in mangroves. We demonstrated that all techniques were robust to tidal inundation, and that four consecutive trap nights were sufficient to detect all taxonomic groups and most species in temperate regions, but that additional nights may be required in subtropical and tropical regions. We recommend RAPTR be used as a biodiversity assessment protocol to identify terrestrial vertebrates in mangroves to fill critical knowledge gaps about these important ecological communities, and one which can potentially be applied to other tidal ecosystems. Such a strategy would further our understanding of the ecological role mangroves play as habitat for terrestrial fauna, and help identify management strategies to aid the conservation of these declining ecosystems.

Full text

ORIGINAL PAPER
Tackling the tide: A rapid assessment protocol to detect
terrestrial vertebrates in mangrove forests
Stefanie M. Rog
1,3
•Rohan H. Clarke
1
•Ernest Minnema
2
•
Carly N. Cook
1
Received: 3 July 2019 / Revised: 23 May 2020 / Accepted: 26 May 2020
ÓSpringer Nature B.V. 2020
Abstract
Globally, the occurrence of terrestrial vertebrates in mangrove forests is poorly docu-
mented, with little empirical data available. This knowledge gap is, at least in part,
explained by the challenging survey conditions typically found in these environments. As
an ecological understanding of ecosystems is essential to guide conservation management
actions, a lack of baseline biodiversity surveys can leave ecosystems vulnerable to
degradation. To address this, we developed and tested a rapid assessment protocol for tidal
regions (RAPTR), that uses a range of techniques to detect mammals, reptiles and
amphibians in mangrove habitat subject to daily tidal inundation. Our approach uses seven
commonly used fauna detection techniques (live traps, camera traps, nocturnal transects,
hair tubes, artificial terrestrial and arboreal refuges, and high-frequency acoustic moni-
toring). RAPTR was implemented over four consecutive nights at each of the 10 sites
spanning temperate to tropical mangrove regions of Australia. We detected 65 species of
terrestrial vertebrates, of which 42 species have not previously been reported in man-
groves. We demonstrated that all techniques were robust to tidal inundation, and that four
consecutive trap nights were sufficient to detect all taxonomic groups and most species in
temperate regions, but that additional nights may be required in subtropical and tropical
regions. We recommend RAPTR be used as a biodiversity assessment protocol to identify
terrestrial vertebrates in mangroves to fill critical knowledge gaps about these important
ecological communities, and one which can potentially be applied to other tidal ecosys-
tems. Such a strategy would further our understanding of the ecological role mangroves
play as habitat for terrestrial fauna, and help identify management strategies to aid the
conservation of these declining ecosystems.
Keywords Coastal Fieldwork Flooded forest Intertidal Inventory Monitoring 
Protected area Survey Swamp
Communicated by Pedro Arago
´n.
This article belongs to the Topical Collection: Coastal and marine biodiversity.
Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10531-020-
02001-w) contains supplementary material, which is available to authorized users.
Extended author information available on the last page of the article
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https://doi.org/10.1007/s10531-020-02001-w(0123456789().,-volV)(0123456789().,-volV)
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Introduction
Biogeographic patterns in biodiversity have interested ecologists for centuries (Wiens and
Donoghue 2004), yet we know more about species richness of some ecosystems than
others. For example, there is often a poor understanding of ecosystems where sampling is
restricted (Anderson 2001; Kier et al. 2005), such as those in regions experiencing political
conflict (Haedrich et al. 2001), or that are physically inaccessible (e.g., mountain cliffs,
Larson et al. 2005 or cave communities, Weinstein and Slaney 1995). With knowledge of
species distributions being a key input for conservation planning (Rondinini et al. 2006),
and an ecological understanding of ecosystems being essential to targeting and resourcing
conservation management actions (Zipkin et al. 2010), the bias in baseline biodiversity
survey effort can leave some ecosystems vulnerable to degradation.
Mangrove forest fauna are among the most poorly surveyed faunal groups within ter-
restrial ecosystems, with most evidence derived from opportunistic species records rather
than systematic survey effort (Rog et al. 2017). Despite mangroves providing a range of
ecosystem services, such as carbon sequestration (Alongi 2016), food provision
(Kathiresan and Rajendran 2002), and erosion mitigation (Mazda et al. 2002), these
ecosystems are under increasing pressure due to aquaculture (Primavera 2006), coastal
development and climate change (Rogers et al. 2016). These pressures have led to wide-
spread and rapid declines, with up to 70% of their global extent lost in recent decades (Giri
et al. 2011). Given these extensive declines in mangroves, there have been increasing
efforts to understand these important ecosystems. Despite mangrove ecosystems spanning
both aquatic and terrestrial realms, research effort has mostly focused on the aquatic
components of these communities, such as crustaceans (Murugan and Anandhi 2016),
benthic species (Nagelkerken et al. 2008), fish and cetaceans (Martin and Da Silva 2004).
The terrestrial fauna, such as the mammals, reptiles and amphibians that utilise mangrove
forests have been largely ignored (Rog et al. 2017); although birds are a notable exception
(Mohd-Azlan and Lawes 2011). To date, the data on the terrestrial species using mangrove
ecosystems have been largely anecdotal (Nowak 2013; Gardner 2016; Rog et al. 2017, but
see Metcalfe 2007), providing little insight into species diversity and the ecological role of
fauna in these systems. This situation calls for more systematic survey effort focused on the
terrestrial assemblages within mangrove forests (Nowak 2013; Gardner 2016; Rog et al.
2017).
The paucity of field studies on the terrestrial fauna within mangrove forests may relate
to the significant challenges these ecosystems pose for ecological surveys (Blench and
Dendo 2007; Hogarth 2015; Luiselli et al. 2015). In particular, tidal inundation and sea-
sonal flooding mean that some traditional terrestrial survey techniques risk fauna drowning
or equipment being lost or damaged. In tropical regions, the presence of large predators,
such as crocodiles and large cats (e.g., Rog et al. 2017), can also pose a risk to researchers.
When combined with the complex branch and root structures of mangrove forests, and the
muddy or silty substrates that make accessing and manoeuvring in these environments
difficult and slow, these attributes present significant barriers to biologists working in these
environments. Challenging survey conditions that impede data collection are not unique to
mangrove forests, and often require traditional survey techniques be adapted to ensure the
safety of field workers, the safety of captured animals, and to minimise the risk of
equipment loss. Currently, no guidelines exist that identify the most appropriate survey
techniques to detect terrestrial vertebrate fauna within mangrove forests. To address this
gap, we developed and implemented a rapid assessment protocol in tidal regions (RAPTR)
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to survey terrestrial mammals, reptiles and amphibians within the tidal range of mangrove
forests. We targeted these groups because they are the most understudied components of
the terrestrial vertebrate community (Nowak 2013; Rog et al. 2017), given that traditional
detection methods, such as live traps, are more vulnerable to inundation than visual surveys
methods, such as those that target birds. We aimed to identify detection techniques that are
safe and effective for use in mangrove forests during periods of tidal inundation. We also
sought to determine the optimal combination of techniques to detect the broadest range of
taxa with the lowest survey effort; and an approach that could be tailored to target specific
taxonomic groups. Our goal was to provide a standardised approach to assessing terrestrial
fauna in mangrove ecosystems that would facilitate cost-effective biodiversity surveys that
improve knowledge within these threatened ecosystems.
Materials and methods
Study system and sites
Mangroves are woody plants that grow in tropical, subtropical and, to a lesser extent,
temperate latitudes along the land-sea interface within bays, estuaries, lagoons, and
backwaters (Mukherjee et al. 2014). Mangrove communities consist of areas that are
regularly inundated by water, as well as those areas inundated during tidal extremes (e.g.,
king tides), where mangrove plants transition into adjoining terrestrial vegetation (i.e., the
ecotone). These ecotonal areas on the landward side of mangrove systems are not always
clearly delineated, and fauna may move freely among these vegetation communities. As
such, we sought sites that represented a diversity of adjoining vegetation communities
(Table 1). Surveys were conducted at ten sites along the eastern seaboard of continental
Australia, along a latitudinal gradient spanning approximately 2500 km, encompassing
temperate, subtropical and tropical regions, and where the tidal range varied between 1 and
13 m. This gradient presented an opportunity to assess detection techniques in systems
representative of the majority of mangrove forests globally. Key attributes of the sites
sampled included: (1) variation in tidal ranges; (2) a latitudinal gradient in floristic species
richness; and (3) an anticipated latitudinal gradient in vertebrate species richness and
community composition.
Survey sites were placed within protected areas on the basis that they held the most
intact vegetation and were anticipated to support diverse communities of terrestrial ver-
tebrates in each region. Sites were spaced at least 75 km apart (Fig. 1).
Data were collected during the austral spring and summer of 2015–2017, these seasons
being the most active periods for the three focal taxonomic groups. Data collection at each
site was conducted during low tides to enable the full intertidal range to be accessible. Data
were collected over four consecutive nights. While it was not possible to avoid all rainfall
events at some sites, data collection was planned to avoid forecasted storm events.
Techniques included
The detection methods included in RAPTR were selected from a list of commonly used
faunal survey techniques for terrestrial mammals, reptiles and amphibians, including both
live trapping and indirect trapping methods. Survey techniques were selected that would
collectively target the complete terrestrial assemblage for the three target groups, including
terrestrial and arboreal species, nocturnal and diurnal species, and small through large-
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bodied species. We scored techniques according to species groups they were likely to
detect, vulnerability to inundation, and as a proxy for cost, the set-up and data processing
time. We then selected the combination of techniques that would target the broadest range
of taxa with the lowest effort to create the most efficient design for field trials (Online
Table 1 Description of survey sites, including their mangrove and adjacent habitat type and floral richness
(for sources see Online Resource S1)
Survey site Mangrove
form
Floral species
richness
mangrove
community
Adjacent broad vegetation
types
Floral species
richness
adjacent
vegetation
(1) Wilsons Promontory
National Park
Fringing 1 Temperate Coastal Saltmarsh 11
(2) French Island
National Park
Fringing 1 Temperate Coastal Saltmarsh 12
(3) Bundeena National
Park
Riverine 2 Swamp Oak Floodplain Forest
(dominated by Casuarina
glauca)
23
(4) Limeburners Creek
National Park
Riverine 2 Swamp Sclerophyll Forest on
Coastal Floodplain
(dominated by Melaleuca
quinquenervia)
Lowland Rainforest on
Floodplain (dominated by
Archontophoenix
cunninghamiana)
51
(5) Bundjalung National
Park
Riverine 1 Dry Sclerophyll Forest &
Woodland (dominated by
Corymbia
intermedia, Eucalyptus
tereticornis)
43
(6) Stradbroke Island
National Park
Fringing 5 Forest on dunes, sand plains,
leached soils (dominated by
Eucalyptus racemosa)
40
(7) Bribie Island National
Park
Riverine 5 Open-forest on coastal alluvium
(dominated by Melaleuca
quinquenervia)
22
(8) Poona National Park Riverine 10 Open-forest on coastal alluvium
(dominated by Melaleuca
quinquenervia)
22
(9) Daintree National
Park
Riverine 26 Complex mesophyll vine forest
on deep fertile soils
Rainforest on foothills of
basalts and alluvium soils
105
(10) Annan River
National Park
Riverine 22 Forest on shallow soil with
impeded drainage (dominated
by Eucalyptus chlorophylla,
Corymbia clarksoniana,
Eucalyptus platyphylla and
Melaleuca viridiflora)
45
When more than one vegetation community was adjoining the site, floral species richness from both
communities was combined. Sites are presented in order of decreasing latitude
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Resource S2). Techniques that could not be effectively implemented in the field within a
5-day timeframe were omitted from further consideration (e.g., canopy camera traps).
Seven techniques were selected for inclusion in the RAPTR (Table 2). Four techniques
were to target mammals: live traps for smaller ground-dwelling species, hair traps for small
to medium arboreal species, camera traps for mammals of all body sizes and high-fre-
quency acoustic monitoring for bats. While hair traps and the bat detector scored poorly on
processing time (e.g., the time and expertise required for processing samples), they were
included on the basis that they filled important gaps in the ability to detect the full fauna
assemblage. Also, they can be deployed safely in relation to trapped animals within
intertidal environments (Online Resource S2). Two techniques were included to specifi-
cally target small to medium-sized reptile and amphibian species: terrestrial and arboreal
artificial refuges, both chosen because they are effective, easy to set-up and rapid to inspect
in the field. Nocturnal transects with a handheld thermal imaging camera (endotherms
only) and spotlight (all species) were included to detect species from all taxonomic groups
that may not be detected using traps. Incidental detections (i.e., sightings, including ‘heard
only’ detections for those species with distinctive calls) and indirect evidence of presence
(e.g., scats and tracks) were also gathered during scouting and set up of the sites.
Pitfall traps (ground-embedded 20 L buckets with removable lids plus drift fence) were
initially included in the protocol to target small ground-dwelling reptiles and amphibians.
To prevent inundation, these traps were placed above the high tide line, and multiple 0.5 m
stakes were inserted diagonally into the substrate to secure the buckets in position.
However, pitfall traps were removed from the protocol after field trials demonstrated that
despite efforts to secure the buckets, hydraulic pressure from groundwater ejected them
from the substrate.
Fig. 1 The location of survey sites in eastern Australia where the effectiveness of the RAPTR approach to
detect terrestrial vertebrates in mangrove forests was evaluated. Numbers correspond to site descriptions
provided in Table 1. The sites span a latitudinal gradient from 39.13°S to 15.56°S. The dashed line
delineates the boundary between temperate and subtropical regions (-30°S) and the solid line delineates
the boundary bet ween subtropical and tropical regions (-23°S) following Corlett (2013)
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Table 2 Techniques and traps with their targets: taxa, body size (small circle: \0.5 kg, medium circle:
0.5–2 kg, large circle: [2 kg) and strata (terrestrial, arboreal)
Technique Method Traps
nights
Target taxa Body size Strata
Live traps
(Closed metal Elliot
traps)
Trap lines of 10 traps,
10 m apart, baited with
peanut butter and oats.
40
Hair tubes (White
20 cm PVC tubes with
sticky tape)
Affixed to tree branches
~1.7 m height, baited
with peanut butter.
24
Camera Traps
(Buckeye, 3 pictures
per trigger).
Placed 30 cm above
ground, baited with
peanut butter and oats.
4
Terrestrial refuges
(Corrugated metal
sheets 50 × 50 cm)
4 trap lines of 10, each
10 m apart. 40
Arboreal refuges
(Closed cell foam
covera70 × 40 cm,
6 mm thick)
Affixed to tree trunks
(~1.5 m height). 20
Bat detector
(Anabat Echo meter)
Affixed to tree trunk
(~1.8 m height),
operated during
nocturnal transects.
1
Night transects
(Thermal Camera,
1000 lumens
spotlight)
Two people; one
operating spotlight, one
operating a thermal
camera, walking at a
speed of ~ 2m/min.
400 m
per
night
Incidental sighti ngs All direct sightings of
animals, and indirect
sign such as tracks and
scats, across the 5 days
of scouting/set up, and
implementation.
n/a
The kangaroo represents all mammal species except bats
a
Closed-cell foam cover is a soft and flexible plastic foam material used in construction
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RAPTR design and implementation
Survey sites were selected to occur within mangrove vegetation that spanned at least
500 m of shoreline, and were located within 2 km of the nearest vehicle access from the
landward side. Sites consisted of a tidal zone (e.g., the area typically inundated twice in
24 h) and an ecotone (Fig. 2). Data collection within each site was based on a block design,
with techniques being replicated across four blocks at each site (Fig. 2). Each of the blocks
was 100 m wide (parallel to the shoreline), and 50 m deep, oriented to the high tide mark,
such that 25 m was frequently inundated and 25 m was within the mangrove ecotone area;
which would only be inundated during king tides (Fig. 2). The high tide mark was
established by scouting two preceding high tides to identify the appropriate placement of
traps to minimise the risk of inundation. Blocks were spaced at least 20 m apart. Four
blocks were used to help estimate the survey effort required to maximise the number of
detections and the ability to estimate species richness across the different regions (Fig. 2).
Each block consisted of 10 terrestrial refuges, 10 live traps, 6 hair tubes, 5 arboreal
refuges. Traps were placed at 10 m intervals. Arboreal traps were placed on randomly
selected stems and branches, informed by the preparatory scouting that identified areas not
inundated during high tide. No more than one trap was deployed per tree. Each block also
included one camera trap, placed at the boundary between the tidal and ecotone area, to
capture individuals moving between these areas. Four, 100 m transects were traversed at
night on foot diagonally across each block.
Only one bat detector was deployed per site, placed in the centre of the four blocks at
the boundary between the tidal and ecotone area (Fig. 2). In total, 40 traps, 4 transects, 4
camera traps and 1 bat detector were deployed per site. Incidental sightings were recorded
across the entire site whenever fieldworkers were present for the duration of the full data
collection period from set-up to pack-up.
The RAPTR approach required 5 full days and two people to implement (excluding
travel to and from the survey sites, and the third person required to monitor for crocodiles
Fig. 2 The RAPTR approach to detect terrestrial vertebrates in mangroves at each site. The first panel shows
a cross-section schematic of each block. The second panel shows an aerial schematic of each block. The
lower panel shows a schematic of the site design. Each block is separated by at least 20 m. Terrestrial
refuges (striped square), live traps (chequered rectangle), camera trap (star), bat detector (bat silhouette),
hair tubes (black circle), arboreal refuges (black rectangle), and nocturnal transect (dashed arrow)
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at tropical sites only). Scouting and set up required one day. The detection techniques and
traps were deployed for four days and four nights. And pack-up occurred during the final
trapping session. The survey effort (the number of days and techniques used) per site was
limited by an imperative that two people could conduct an entire protocol within 5 days,
seeking a compromise between detection probability and survey effort.
Species identification
Species identification for live captures and camera trap images followed Menkhorst and
Knight (2001) and Cogger (2014). High-frequency sonograms derived from bat recordings
were viewed in Kaleidoscope Pro 4 (Wildlife Acoustics 2015), identified by a single expert
familiar with the identification of echolocation calls of eastern Australian Microchiropteran
bats, and then verified by independent experts with access to reference libraries. Any
recordings that were impossible to be identified to species level owing to poor recording
quality, or separation of calls, were omitted. Hairs collected from hair tubes were identified
to species by an Australian expert based on the identification of hair cross-sections.
The mangrove floral richness at each site was estimated following Duke (2006),
together with targeted literature searches for vegetation assessments at each site (Online
Resource S1). To identify the adjacent vegetation community bordering each study site we
used vegetation maps from management plans for each site as well as relevant vegetation
condition benchmarks to identify the floral richness of the vegetation communities (see
Online Resource S1).
Evaluation of the RAPTR
Each technique used in RAPTR was assessed in relation to success at avoiding inundation,
and the overall number and taxonomic composition of the species detected. The RAPTR as
a whole was evaluated according to the ability to detect species of different body sizes
(small B0.5 kg, medium-sized between 0.5–2 kg, large C2 kg) and across vegetation
strata (e.g., terrestrial or arboreal, based on their general ecology) and how well the
taxonomic composition of species detected matched global patterns in vertebrate taxa
observed in mangrove forests (Rog et al. 2017). Any redundancy in the species detected
(i.e., the combination of techniques required for maximum species detections) was also
assessed.
The efficiency of the protocol (trap nights and the number of blocks per survey site) was
assessed according to: (1) whether an accumulation curve of species richness has
approximately plateaued by the fourth trap night; and (2) whether all survey blocks were
required to detect the full complement of species.
We were also interested in whether the previously reported correlation between faunal
richness and the mangrove floral species richness was observed across sites (see Rog et al.
2017). Most species known to use mangrove forests are thought to be facultative users of
the vegetation community, moving in and out of adjacent habitats primarily to utilise food
resources (Rog et al. 2017). Therefore, we calculated Pearson’s correlation coefficients
between faunal richness and the floral richness at a site. This was done for both the
mangrove community and the adjacent vegetation community, because the faunal species
richness of the adjacent habitats may influence any observed relationship.
We assessed whether there were differences in the mean number of species detected
across regions using analysis of variance (ANOVA).
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Results
Effectiveness of RAPTR
We detected 65 species of terrestrial vertebrate across the 10 sites (Tables 3and 4). Of
these, 42 species had not previously been reported in mangroves (Rog et al. 2017; Table 4;
Online Resource S3). Selecting the placement of traps after assessing the tidal range was
sufficient to ensure all techniques avoided inundation across all three regions, with no
inundation events recorded during 5160 trap nights. Mammals were the most frequently
detected taxa (64% of detections; n = 42 species), followed by reptiles (29%; n = 19) and
amphibians (6%; n = 4). Incidental sightings generated the largest number of species
detections, while the bat detector contributed the largest number of unique species (i.e.,
those not detected by any other technique; Table 3). Four of the eight techniques detected
multiple taxonomic groups (Table 3).
All target taxa and subgroups were detected by at least one technique, except for
medium and large-bodied arboreal reptiles (e.g., tree snakes and varanids, Table 5). Four of
the eight techniques detected all target taxonomic groups predicted, and three of these
techniques detected additional groups that were not anticipated (e.g., reptiles by camera
traps). Some techniques failed to detect some of the target taxa (e.g., terrestrial and
arboreal refuges did not detect amphibians) or subgroups (e.g., nocturnal transects did not
detect large arboreal reptiles). While several of the techniques detected small and medium-
sized species, larger-bodied species of mammals and reptiles were typically detected by
only a single technique. The largest number of target groups was detected through inci-
dental sightings (Table 5).
Mammals
All six techniques that targeted mammals (live traps, bat detector, camera traps, hair tubes,
nocturnal transects and incidental sightings) detected representatives of this group
(Table 5). Incidental sightings of mammals include visual detections of live animals as
well as indirect indicators of presence, such as skulls, and distinctive tracks and scats.
Despite nocturnal transects being predicted to detect large arboreal mammals, this sub-
group was only detected through incidental sightings (Table 5). Live traps, hair tubes and
camera traps were effective at detecting mammals in both the terrestrial and arboreal strata
(e.g., arboreal possums by camera traps; Table 5).
Reptiles
The four techniques that targeted reptiles all detected representatives of this group. While
not anticipated, camera traps also detected reptiles (Table 5). Terrestrial refuges proved
important to sample small reptiles not detected by other techniques (Fig. 3). However,
terrestrial refuges did not generate detections of medium-sized ground-dwelling reptiles,
which were instead detected through camera traps and incidental sightings (Table 5).
Amphibians
Nocturnal transects and incidental sighting detected the largest number of amphibian
species, including those not detected by other techniques (Table 5). Despite expectations,
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Table 3 The number of species detected across all 10 survey sites in mangroves, showing the total number of species detected per technique, and the unique species detected
(i.e., species not detected by other techniques)
Incidental, e.g., visual, scat,
track
Bat
detector
Live
traps
Nocturnal
transects
Camera
traps
Hair
tubes
Terrestrial
refuges
Arboreal
refuges
Total # species detected 36 12 8 18 11 8 7 3
Frog species (unique frog species) 3(25%) – 1(0%) 3(25%) – – ND ND
Reptiles species (unique reptile
species)
15 (26%) – – 5(5%) 1(0%) – 7(0%) 3(0%)
Mammal species (unique mammal
species)
18 (7%) 12
(100%)
7(7%) 10 (7%) 10 (0%) 8(3.5%) – –
A dash (–) indicates that the technique was not expected to detect a taxonomic group. ND indicates that a technique was predicted to detect this taxonomic group but failed to
do so
Bold was used to distinguish the number of species from the percentage
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Table 4 Species detected by RAPTR across ten mangroves sites in temperate, subtropical, and tropical
eastern Australia
Family group Common name Species Reported in
Australian
mangroves by Rog
et al. 2017
Amphibians
Frog Cane toad Bufo marinus
Frog Australian green tree frog Litoria caerulea
Frog Eastern dwarf tree frog Litoria fallax
Frog Rocket frog Litoria nasuta
Reptiles
Crocodile Saltwater crocodile Crocodylus porosus H
Lizard Closed-litter rainbow-skink Carlia longipes
Lizard Shaded-litter rainbow-skink Carlia munda
Lizard Brown bicarinate rainbow-skink Carlia storri
Lizard Snake eyed skink sp. Cryptoblepharus pulcher
Lizard Snake eyed skink sp. Cryptoblepharus virgatus
Lizard Barr sided skink Eulamprus tenuis
Lizard Dubious detella Gehyra dubia
Lizard House gecko Hemidactylus frenatus
Lizard Sunskink sp. Lamphropholis amiculata
Lizard Sunskink sp. Lampropholis delicata
Lizard Mourning gecko Leptodactylus lugubris H
Lizard Glossy grass skink Pseudemoia rawlinsoni
Lizard Pale lipped shade skink Saproscincus basiliscus
Lizard Lace monitor Varanus varius
Lizard Burton’s legless lizard Lialis burtonis H
Snake Spotted python Anteresia maculosa
Snake Common tree snake Dendrelaphis punctulatus H
Snake Marsh snake Hemiaspis signata
Mammals
Bat White striped free-tailed bat Austronomus australis
Bat Gould’s wattled Bat Chalinolobus gouldii H
Bat Chocolate wattled bat Chalinolobus morio
Bat Eastern false pipistrelle Falsistrellus tasmaniensis
Bat Little bentwing bat Miniopterus australis H
Bat Eastern bentwing bat sp. Miniopterus orianae
oceanensis
Bat Eastern bentwing bat sp. Mormopterus lumsdenae
Bat Eastern freetail bat Mormopterus ridei
Bat Southern myotis Myotis macropus
Bat Black flying fox Pteropus alecto H
Bat Eastern horseshoe bat Rhinolophus megaphyllus
Bat Little broad-nosed bat Scotorepens greyii H
Bat Eastern forest bat Vespadelus pumilus
Canid Dingo Canis lupus dingo H
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terrestrial and arboreal artificial refuges, which targeted amphibians, were not successful
(Table 5); by contrast, live traps unexpectedly detected ground-dwelling amphibians
(Table 3).
The mean number of species detected varied across regions, with more species detected
in the tropical region (l= 20.5 ±1.93 SE) when compared with the subtropical
(l= 11.5 ±1.09 SE) and temperate (l= 8.5 ±1.28 SE) regions. However, these patterns
were not statically significant (F = 2.96; df = 2; p = 0.110) given the substantial variation
in the number of species detected by technique within regions (Fig. 3). Incidental sightings
consistently detected the largest number of species across all regions.
At the regional level, there were several techniques that failed to detect any species.
These included nocturnal transects (no reptiles were detected in the temperate region nor
amphibians in the tropics) and camera traps (no reptiles were detected in subtropical or
tropical regions) (Online Resource S4).
Table 4 continued
Family group Common name Species Reported in
Australian
mangroves by Rog
et al. 2017
Canid Domestic dog Canus lupus
Canid Fox Vulpus vulpus
Felid Domestic cat Felis catus H
Lagomorph European rabbit Oryctolagus cuniculus
Marsupial Brown antechinus Antechinus stuartii
Marsupial Bennett’s tree kangaroo Dendrolagus bennettianus
Marsupial Agile wallaby Macropus agilis H
Marsupial Eastern grey kangaroo Macropus giganteus
Marsupial Sugar glider Petaurus breviceps
Marsupial Brush tailed phascogale Phascogale tapoatafa
Marsupial Common planigale Planigale maculata H
Marsupial Eastern Ringtail possum Pseudocheirus peregrinus
Marsupial Common brushtail possum Trichosurus vulpecula H
Marsupial Swamp wallaby Wallabia bicolor H
Rodent Common water rat Hydromys chrysogaster H
Rodent Grassland melomys Melomys burtoni H
Rodent Fawn footed melomys Melomys cervinipes H
Rodent House mouse Mus musculus H
Rodent Bush rat Rattus fuscipes H
Rodent Swamp rat Rattus lutreolus
Rodent Black rat Rattus rattus
Rodent Water mouse Xeromys myoides H
Rodent Delicate mouse Pseudomys delicatulus H
Rodent Giant white-tailed rat Uromys caudimaculatus H
Ungulate Hog deer Axis porcinus H
Ungulate Cow (domestic) Bos taurus
Ungulate Rusa deer Rusa timorensis
Ungulate Wild pig Sus scrofa
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Survey effort
No novel species (those not detected on previous nights) were detected on the fourth night
of data collection in the temperate region. By contrast, novel species continued to be
Table 5 Target groups detected by techniques in RAPTR
Terrestrial and arboreal refer to the target strata. Shaded cells indicate the technique was not predicted to
detect the target group. A indicates members of the relevant group were detected, a indicates the target
group was not detected contrary to expectations. See Online Resource S3, for species detected per technique
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detected on the fourth night in the subtropical and tropical sites (Fig. 4A). These novel
species (mammals and reptiles) were detected by several techniques (nocturnal transects,
terrestrial refuges and camera traps) in both the subtropical and tropical regions. We
provide incidental sightings as a separate plot (Fig. 4B) as incidental sightings offer insight
into the number of species detected while checking traps, as well as during site scouting
and set up (day 0). Sightings of new species ceased after day 2 in the temperate region and
after day 3 in the subtropical and tropical regions (Fig. 4B).
The RAPTR, four-block design was required to detect the full complement of species at
all but one site in the temperate region (mean number of species detected per block:
temperate—l= 1.4 ±0.23 SE; subtropical—l= 1.6 ±0.90 SE; tropical—
l= 1.8 ±0.44 SE). The number of blocks that detected any species was highly variable
among the different techniques and across regions (Fig. 5).
Relationships between terrestrial vertebrate richness and available habitat
While we observed a moderate positive correlation between terrestrial vertebrate richness
and mangrove plant richness in line with that reported globally (Rog et al. 2017; r = 0.56),
this relationship was not statistically significant (r = 0.55; p = 0.101; n = 10; R
2
= 0.300).
Contrary to expectations, only a weak positive correlation was observed between terrestrial
vertebrate richness and floral species richness of the adjacent terrestrial vegetation com-
munities among the field sites in Australia, again not statistically significant (r = 0.26;
p = 0.255; n = 10; R
2
= 0.158) (Table 6).
Fig. 3 Mean number of terrestrial vertebrate species detected per technique in mangrove forests within
5 days in temperate (grey bars, n = 4 sites), subtropical (black bars, n = 4 sites) and tropical (white bars,
n = 2 sites) regions of eastern Australia
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Discussion
While mangrove forests are a challenging environment to survey, we demonstrate the value
of a rapid assessment protocol in tidal regions (RAPTR), that employs a range of common
field survey techniques to successfully detect a wide range of terrestrial vertebrates in these
systems. The value of RAPTR to expand our knowledge of the vertebrates that use these
communities is demonstrated by the number of species we detected that had not previously
been reported in mangroves. Across only 10 sites in Australia, RAPTR increased the
number of species known to use mangroves globally by almost 10% (i.e., 42 species added
to an existing database of 463 species collated by Rog et al. 2017). Such an outcome
demonstrates the value of on-ground assessments relative to what have otherwise mainly
been anecdotal occurrence records (Rog et al. 2017).
Effectiveness of RAPTR
We found that all of the techniques included in the protocol were effective at detecting
multiple taxa within just four trap nights and that all target taxonomic groups were
detected, with the exception of large arboreal reptiles. Night transects and incidental
sightings detected the widest range of species across taxonomic groups and detected
unique species for all groups. Artificial refuges were the least successful technique with
0
2
4
6
8
10
12
14
1234
Cummulave mean species richness
Trap nights
0
2
4
6
8
10
12
14
01234
Cummulave mean species richness
Trap nights
AB
Fig. 4 Cumulative species richness for terrestrial vertebrate species detected with RAPTR in mangrove
forests in temperate (grey line), subtropical (black line) and tropical (dashed line) regions of eastern
Australia. ASpecies detected per trap night (including live traps, terrestrial and arboreal refuges, camera
traps and nocturnal transects). Hair traps and the bat detector were excluded from this figure as no distinction
could be made between species detected per day. BSpecies detected incidentally. This plot commences at
day 0 to account for incidental sightings that were obtained prior to trapping events (during scouting and set-
up)
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regards to species richness. Still, we include it in RAPTR because unique species were
detected through the use of terrestrial or arboreal refuges at individual sites (see Online
Resource S3), playing an important role in detecting cryptic reptiles (Bell 2009).
Table 6 The richness of terrestrial vertebrate fauna, mangrove plants and adjacent habitat (vegetation
community) on each survey site in eastern Australia
Location Terrestrial vertebrate
species richness
Mangrove floral
species richness
Adjacent habitat
floral species richness
Temperate
Site 1 8 1 11
Site 2 5 1 12
Site 3 8 2 23
Site 4 13 2 51
Subtropical
Site 5 8 1 43
Site 6 12 5 40
Site 7 19 5 22
Site 8 14 10 22
Tropical
Site 9 13 26 105
Site 10 22 22 45
Fig. 5 The mean number of blocks in which a technique within RAPTR detected at least one mammal,
reptile or amphibian species within temperate (grey bars), subtropical (black bars) and tropical (white bars)
mangrove regions of eastern Australia
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In the absence of data on the full faunal species assemblage at each site, it was not
possible to determine what proportion of species RAPTR did not detect. There are several
additional species (2 frogs, 4 reptiles, 11 bats and 6 additional terrestrial mammals) that
have been anecdotally reported to use mangrove (Rog et al. 2017) and have distributions
that overlap our field sites. Added to the fact that the species accumulation curves from
tropical and subtropical regions had not plateaued (Fig. 4); likely, a 5-day RAPTR was not
sufficient to detect all species present. Nevertheless, patterns of species richness observed
in this study were consistent with global patterns for mangrove forests, with terrestrial
vertebrate species richness being higher at lower latitudes (Rog et al. 2017). The taxonomic
groups detected by RAPTR also reflected patterns observed globally (Rog et al. 2017; 68%
mammals, 25% reptiles and 5.6% amphibians), with mammals being the most frequently
detected taxa across all regions, accounting for 64% of all species detected, followed by
reptiles (29%) and amphibians (6%). Such alignment suggests that RAPTR is an appro-
priate tool for rapid biodiversity assessments in mangrove systems globally.
Mammals
Where mammals are the target for data collection, our findings suggest that the optimal
combination of survey techniques would be to use nocturnal transects, incidental sightings
and a bat detector, combined with live traps to detect small terrestrial mammal species
(Table 5). Hair traps detected similar species to live traps. While hair traps required more
extended processing times (Online Resource S3), they do present a possible substitute for
live traps where the latter cannot be safely placed on the ground. Combining multiple
techniques to maximise known species richness of mammals is also the recommended
approach within fully terrestrial systems (e.g., Rockhill et al. 2016; Storm 2017; Garden
et al. 2007).
Reptiles and amphibians
Little is known about detection techniques for reptiles and amphibians in mangrove forests.
Globally these taxa are reported to be uncommon in mangroves (Rog et al. 2017). Nev-
ertheless, it remains unclear to what extent detectability also shapes our understanding of
reptile and amphibian species richness in mangroves. We found that nocturnal transects
and incidental sightings were most successful at detecting both reptiles and amphibians,
and so recommend these techniques if targeting these taxa (Tables 3and 5). Studies
evaluating the effectiveness of terrestrial herpetological survey techniques show similar
results regarding the efficiency of these techniques (Sung et al. 2011; Hsu et al. 2005; Doan
2003). One exception to this is pitfall traps, which could not be successfully deployed in
mangrove forest due to the hydraulic pressure, but which provide a valuable approach to
detecting reptile species in other terrestrial environments (Corn and Bury 1990). The
capacity of artificial refuges to detect terrestrial reptiles offers a partial alternative to pitfall
traps.
While artificial refuges are unlikely to be effective at detecting subterranean species
assemblage (e.g., blind snakes and sand swimmers) that do not shelter under surface debris,
these groups are likely to be absent in waterlogged mangrove soils. Extending the survey to
allow for an acclimatisation period prior to sampling (O’Donnell and Hoare 2012) may
also improve the detection rates of artificial cover objects. While our goal was to develop
an effective and efficient protocol, additional time for acclimation may be beneficial where
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surveys target reptiles and amphibians. Further study is required to determine whether the
reptile and amphibian fauna in mangrove forests are genuinely depauperate, or simply
harder to detect. The lack of understory in mangrove communities may provide little
habitat for this assemblage (Luiselli and Akani 2002).
Efficiency of RAPTR
Through the implementation of RAPTR, our study provides some key recommendations
for those seeking to design the most efficient approach to detecting terrestrial vertebrates in
mangroves. Where the objective is a census of species present, our data suggest it may be
important to tailor the survey effort to the predicted species richness of the region. We
found that a 4-day protocol was sufficient in temperate regions (Fig. 4), but that in tropical
and subtropical regions additional species were still being detected on the fourth night
(Fig. 4). While more research is needed to inform decisions around optimal survey effort in
regions with higher species richness, RAPTR implemented over 5 days offers value in
improving our understanding of the wide range of terrestrial fauna that uses mangrove
communities. Most species were detected within just one or two blocks across regions, and
all techniques detected species that would not otherwise be detected. Our data therefore
suggest that reducing the number of blocks in the RAPTR design, or the number of
techniques used, likely impacts estimates of species richness.
Where the objective of data collection is to detect the largest number of species, the
most efficient technique would be to use nocturnal transects, combined with incidental
sightings. Both techniques are well-recognised for their capacity to locate species that may
not otherwise be detected (Larsen 2016). These two techniques consistently detected the
largest number species across all regions in our study and the broadest range of target taxa.
While both techniques require the active involvement of skilled personnel, they require
little equipment (thermal imaging camera and spotlight for nocturnal transects) and min-
imal processing time. Most novel incidental sightings were obtained during the first three
days of the sampling, likely because of continuous human activity during the survey
period. Incidental sightings are obtained with no material cost with regards to personnel
time, so should always be incorporated in the assessment protocol. Therefore, where site
managers lack the resources to conduct the RAPTR as described, our data suggest that
doing site visits during the day (and preferable also at night) will contribute valuable
insight into the presence of terrestrial vertebrates in mangrove forests.
Where the objective of data collection is to detect specific groups, our data provide
direction as to which techniques would be most efficient. When selecting the most efficient
techniques, it is essential to consider the costs of purchasing equipment, processing
samples (e.g., identification of hair samples and screening photos) and personnel time.
Furthermore, some techniques cannot detect the full complement of species within a target
group. For example, while nocturnal transects and incidental sightings were effective at
detecting small mammals in general, they were poor at detecting some groups, such as
rodents and bats (Online Resource S3). Relying on these methods alone to detect mammals
would not only underestimate mammal species richness but also introduce systematic bias.
Therefore, the optimal survey design for each taxon needs to consider both effectiveness
and efficiency.
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Improving knowledge of vertebrates in mangroves
While RAPTR has contributed substantial new information on the vertebrate species within
mangroves, variations to the design of the protocol could be tested to further understand
variation in species detection. For example, using novel baits (e.g., sardines) within the
live, hair and camera traps may attract a broader range of small mammal species. Likewise,
using an additional bat detector or recording calls throughout the night might further
increase the number of bat species detected (Skalak et al. 2012). The influence of tides and
the associated moon phases on both the presence and detectability of different species in
mangroves also requires further investigation (Spence-Bailey et al. 2010). Despite noc-
turnal transects being predicted to detect large arboreal mammals, this subgroup was only
detected through incidental sightings (Table 5). This paucity of detections may reflect a
genuine scarcity of large arboreal mammals within Australia. Finally, seasonal factors
should also be considered where the goal is to accumulate more complete species inven-
tories (Haugaasen and Peres 2005). In sites with marked seasonal variation in resources
(e.g., variation in fruit and nectar availability), multiple rapid assessments undertaken at
different times of the year may be required (Gardner 2016; Rog et al. 2017).
Understanding the species present in mangroves is an essential step in improving our
knowledge of these ecosystems. However, surveys that simply detect species provide little
insight as to how these species utilise mangrove communities. In our study, floral species
richness of the adjacent habitat was a less effective predictor of faunal richness than was
the floral richness of mangrove species. Nonetheless, previous research suggests that most
fauna in mangroves are facultative users that move in and out of mangrove to exploit
specific resources (Rog et al. 2017), making it important to consider the fauna in adjacent
habitat. In regions where field assessments in mangroves are not possible, fauna surveys in
adjacent vegetation may provide an indirect measure of species richness in mangroves to
guide conservation priorities.
Conclusions
Our rapid assessment protocol in tidal regions (RAPTR) demonstrates that data on ter-
restrial fauna in mangrove forests can be rapidly collected to extend the largely anecdotal,
existing species records. The routine application of RAPTR as a protocol would promote
more systematic, empirical surveys of terrestrial vertebrates, reducing the bias in baseline
biodiversity datasets that are crucial to an improved understanding of mangrove ecology.
Such an approach would ensure managers are well-positioned to inform conservation
management actions and implement adequate protection. An important parallel step is to
adapt RAPTR to explore the ecological role of terrestrial vertebrates in mangroves. With
an emphasis on resource use and the provision of ecosystem services, such research would
provide a deeper understanding of the co-dependence of these forests and their inhabitants.
Acknowledgements We thank the Quandamooka, Kuku Yalanji and Yuka Baja Traditional Owners for
allowing us on their land and national parks staff from Wilsons Promontory, French Island, Bundeena,
Limeburners Creek, Bundjalung, Stradbroke, Bribie Island, Poona, Daintree and Annan River National
Parks for their assistance. D. Chapple, B. Triggs and A. Lacostada assisted with species identifications. R. J.
Pilgrim and L. C. Booth provided invaluable field assistance.
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Data availability The datasets generated during and/or analysed during the current study are available from
the corresponding author on reasonable request.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of interest.
Ethics approval This research was partly funded by a The Holsworth Research Endowment and a Paddy
Pallin Science Grant, and conducted under appropriate State wildlife permits and animal ethics approval.
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Affiliations
Stefanie M. Rog
1,3
•Rohan H. Clarke
1
•Ernest Minnema
2
•
Carly N. Cook
1
&Stefanie M. Rog
rog.stefanie@gmail.com
1
School of Biological Sciences, Monash University, 25 Rainforest Walk, Melbourne 3800, Australia
2
University of Georgia Costa Rica Campus, Apartado 108-5655, Santa Elena, Monteverde,
Puntarenas, Costa Rica
3
Wetlands International, Horapark 9, 6717 LZ Ede, The Netherlands
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