Goal-Directed Travel in the Nocturnal Javan Slow Loris (Nycticebus javanicus)

Round 1

Reviewer 1 Report

In general, this is a relevant and well-written manuscript as it presents detailed spatial data on a relatively poorly-known primate group. 

 

Introduction:

-Reference on how translocated primates used spatial information in newly-known habitats is still missing.

-In addition, as the manuscript refers also to primate translocation, a further examination needs to be added on how forest structure and habitat preference are used to explore potential translocation needs.     

Discussion:

-Compare the parameter of spatial cognition  (e.g. circuity index, reused of trees, etc) with other nocturnal primates (mouse lemurs, Aotus, etc). Information on movement ecology in nocturnal primates is scant, and this article might shed even more light on this issue if addressed comparatively.

 

Major concern:

-Looking at the discussion, I am not sure to what extent “ forest structure sensu lato” determines the use of space in lorises, and primates in general. There are many other factors that relate to primate ranging (presence of other primate groups or species, predation, anthropic modification, etc). In fact, forest structure is quite a vast realm that involves, e.g.,  ranging from different kinds of habitats (primary forest, shrubs, etc) or the size of trees to physical features such as the presence of water bodies, slopes, etc. Thus, what is the size of trees commonly used trees by lorises, and how different do these animals use different types of habitats, do rivers constrain movement, and do lorises use slopes as spatial references for navigation? These issues are not addressed in the discussion if "forest structure" is actually considered the core of this text.   Decision: Accept with major revision.

Author Response

Please note we also have changed the title as per reviewers' requests but we cannot do this on the system itself at this time.

Author Response File: Author Response.docx

Reviewer 2 Report

This paper analyzes Javan slow loris movement ecology and puts it in the context of release sites for translocation. I enjoyed reading it and I think it will be a useful addition to the literature. I do have a few comments and suggestions though to make the paper even better.

The introduction is well-written overall and sets up the study nicely. There do seem to be some places where multiple spaces are placed between words, rather than just one, but this is a minor thing.

 

The methods are also clear. More information is needed for a few analyses. First, in how “goal locations” were defined. Were gum feeding trees of all size considered a goal? Or did the tree have to be above a certain DBH? Or did it have to be previously fed upon by the lorises? I am just wondering if there were any criteria here, otherwise it seems like an erroneously large number of trees could be goal locations. It is also not totally clear what map the heuristic routes model was based on (lines 115-122). Was a map of all possible gum feeding trees in the area available from previous research? The stated data that were being collected for this study focus on places where the lorises went but the model is based on where they could theoretically go, so it needs to be stated how this is known.

 

One thing that I thought would be a good addition to the Results is whether or not males and females differed in route overlap (lines 160-161). In Table 3, it looks like females may be more consistent in route use than males. This could be measured statistically using a linear mixed model to control for individual and looking at overlap relative to sex. Actually, overall NPL could also be compared between the sexes this way to say definitively that there is no difference (line 127).

 

The Discussion brings up all relevant points. However, it would be great if it was noted somewhere whether the lorises ever came to the ground to move between trees/patches (around line 231 perhaps). If not, then tree connectivity would certainly be key for their release sites. If so, how far would they move on the ground and still feel comfortable?

 

Minor comments:

 

Lines 19-20 – Consider modifying so that “structure” is not used twice in one sentence.

Line 21 – Delete “the” before “movement”.

Line 58 – It seems a final verb is missing from this sentence. Perhaps “feeding and foraging needs” would read better.

Lines 64-66 – Commas between the numbered aims of the study would be nice. I also think the “(4)” should be moved before “by”.

Line 67 – Add “that” after “confirm”.

Lines 82-85 – A map of the study area would be useful.

Line 99 – Change “it” to “this”.

Line 115 – Change “it encountered” to “encountering”. On a different note, this line seems to be in a different size text.

Line 116 – Change “at” to “as”.

Lines 133-134 – From the lines here it is unclear if they only revisited four tree species or if they revisited more but only four were identified to the genus and species. Please clarify.

Line 140 – Pluralize “tree”.

Lines 156-157 – For a behaviour to be associated with a change-point, did it have to occur before, right afterwards, or during? This should be stated in the methods.

Line 174 – “Javan” is misspelled.

Line 189 – Change “they” to “individuals and groups”.

Line 204 – Add a comma after “range”.

Line 210 – Add a comma after “taxa”.

 

Author Response

Please note we also have changed the title as per reviewers' requests but we cannot do this on the system itself at this time.

Author Response File: Author Response.docx

Reviewer 3 Report

This is an interesting study that explores the movement patterns of Javan slow lorises to determine how they navigate throughout their home ranges.  Given that the study animals are small, nocturnal primates, the data set is robust, as it covers an entire study year. Furthermore, the results are important for broadening our understanding of how different animals have adapted to efficiently forage in their environments.  The paper should be of particular interest to researchers who study spatial cognition.

That said, I feel that the authors’ title and introduction do not match the study. For example, the title uses the phrase “Forest structure,” but I think “forest structure” implies the actual physical structure of a habitat - the density of vegetation in the understory, the diversity of trees, the height of the canopy, the DBH of trees, etc. This type of data is not presented in this paper. Instead, what the authors focused on was the location of feeding trees. And, they found that the location of feeding sites was the primary influence on loris movement patterns.  So, the title could be “The location of food resources influences movement patterns,” or "repeated use of foraging trees affects movement patterns."

In addition, the introduction focuses on wildlife translocations.  However, the study is not on translocated animals. My suggestion, therefore, is to move all this information on translocations to the Discussion.  The data in this paper certainly can be used to help make better decisions as to where lorises can be successfully translocated, and to point out what additional research is needed to better plan translocations, but it was not the focus of the study. 

Instead, the paper is on the ranging behavior of lorises, and their spatial cognition.  So, the introduction should focus on spatial memory and foraging (briefly mentioned in paragraph 2). It should review the range of “mental maps” and “memory skills” that have been found across different types of animals. It also could present data on the feeding behavior of the lorises, given that the authors predict the location of feeding sites will be important. With this new focus, the authors could present some hypotheses and predictions on loris mental maps, and then present the results and discussion as tests of those predictions.

I also think that the authors should present data on the home ranges of the animals, in this way, the reader knows the context for the night path lengths that are given.  A 500m night path in a home range of 100 ha is very different than that same distance night path in a home range of 10 ha. They should also include information in the methods on how those home ranges were calculated (currently only mentioned in the legend of Figure 1).

The authors state that Figure 1 displays a sample nightly route of one male and one female loris, but it appears to only have the route of one male.

I also would recommend adding a figure that shows one animal’s use of its home range over the course of the study.  In that way, it will be easier to visualize the types of change points and route overlaps referred to in Table 3 and on page 5. 

On page 5, you state that most change-points were associated with specific behaviors.  Then, you go on to state that you were unable to identify and “biological meaningful associations” for two others.  You should clarify that you were unable to find any “behavior” that was associated with those change points.  After all, you did not measure other things, like what I would consider the “forest structure” at those points. For example, perhaps those points had different vegetation that required moving in a certain direction (e.g. a treefall that needed to be avoided).  Those would be biologically meaningful (lack of appropriate structural supports for movement, increased predation risk, etc.), but not behavioral.

I also think you could do some additional analyses that would be important for future translocation studies. For example, how did feeding tree density affect home range size and nightly path length?  That is did animals with many of the repeatedly use trees have smaller home ranges than those with fewer?  Was there a minimum number of trees across groups?  This data would help inform people planning translocations about minimum habitat sizes needed for an individual based on the density of the loris’s key feeding trees in that habitat. I think the authors can do more detailed comparisons of the different individuals in their study, to try to determine what factors contributed to their differences (or similarities).

Minor edits (not all of which may not be needed if the paper is reorganized as I suggest above).

Line 21 – what does “truly” mean?

Line 38- Animals possess… their home range

Lines 54-56 – Make the phrase on increased success its own paragraph and explain why. Rephrase the rest of the sentence, something like “There has been little work done to…”

Line 57- connectivity between what?

Line 57- explain what is you mean by structure – density of food resources, tree diversity, etc. As stated above, I think you need to differentiate between general forest structure and the density and location of loris feeding trees.

Line 89- how were full night paths obtained if data was collected on two different focal animals in the two shifts each night?

Line 93 – what was the mean error of the GPS in this forest?

Line 103- GPS

Table titles – seems unnecessary to state “in Ciaganti, Java, Indonesia” in every table title, as this is the only site used in this study

Line 142-143 – cut this, as “revisited” is defined in the methods

 Figure 1 – Put the meters under the scale bar.  What do the letters and number above the scale bar refer to?

Line 174- cut the “e”

Line 194- include the study period “during this year-long study”

Line 203 and 205- see comments above.  I do not think you characterize forest structure in this paper.

Line 234- what do you mean by “ever-changing environment”?  Do you mean due to human disturbance? Aren’t all environments always changing? I assume you mean dramatic change due to activities such as logging, agriculture, etc.

Author Response

Please note we also have changed the title as per reviewers' requests but we cannot do this on the system itself at this time.

Author Response File: Author Response.docx

Round 2

Reviewer 1 Report

Accept in present form.

Author Response

We thank the reviewers for reevaluating this work and all the comments which have helped to improve the article. 

Reviewer 3 Report

I commend the authors on the substantial changes they made to their manuscript. It is much improved as the authors changed the focus of the introduction, clarified their methods, presented new graphics and data, and reworked the discussion.

I have some further suggestions listed below.  These are mostly minor suggestions to clarify the meaning of some sentences, although a few contain some more substantive questions.

Line 30- “we measured their frequency” refers to what?  I think there is a word or phrase missing, as it is not clear what “their” refers to

Line 31- keep in past tense – changed

Line 33- confusing to end last sentence with tree species, and then begin the next sentence with “this species” and it refers to the lorises.  I would replace “species” with “The lorises display”

Line 67-68- I would change “used regularly in discussions” to something like “provides insights into”

Line 84- not just what will be the most efficient option, but also the one that is cognitively possible for the species, based on phylogeny and cognitive ability (e.g. memory), no?

Line 93- rephrase to something like, “and their movement patterns fit with the expectations of a route-based cognitive map”

Line 96- put a colon after “specialization” rather than a comma, and then cut “where”

Line 98 – I am not sure what is meant by “displays flexibility in a setting”? Do you mean dietary flexibility, habitat use?  Can you clarify?

Line 100 – “facilitate access to” means “find and return to”?

Line 100-101 I would move this to the end of the paragraph and add a sentence that indicates the widespread importance of gummivory among primates with a citation (such as Cabana’s review of gummivory).

Line 110- here too the use of “their frequency” is unclear, do you mean “the frequency of use of locations used repeatedly”?

Line 114- “the efficiency” refers to path length?  Please clarify

Line 114- I think this needs to be broken into three separate predictions, which if supported would provide evidence for a route-based cognitive map

A.      Actual travel paths shorter than randomly simulated paths

B.      Reuse of paths between locations

C.       Use of nodes where animals can switch routes

Line 137- I think I would move this sentence to the discussion.  It seems out of place here.

Line 153- move “a”to before “Map of the study..”, move “b” to “and a satellite image”

Line 154- I would cut “by the Little Fireface Project”

Line 190 – stay in past tense “ they encountered”

Line 192-194 I found this sentence to be confusing. Can you clarify? Do you mean that lorises might be able to see locations from certain distances which would allow them to move “off route”?  That is they would stay “on route” until they saw the target?

Line 248- Figure 2 appears to be at very low resolution, please increase to make it possible to see the dark circles.

Line 287- usually published studies are in the present tense, so  “also structure…move…”

Line 291 – “The most plausible method that lorises use to revisit gouged sites is to rely on their….”

Line 300- “thus it is likely that the Javan slow loris uses a more robust route network than we detected in this study…”

Line 328- I think that it is hypothetically possible that an individual’s routes would cross its whole home range making it unnecessary to remember the phenological data as the routes would pass by all potential food sources. It is unlikely though.  It seems like you should suggest that further work is needed to determine how routes may shift monthly or annually in response to changes in resource availability over time.

Line 330-339 – This paragraph should go at the beginning of the discussion. This is the “null model” so to speak, so first explain why you reject tt, and then explore the alternatives.

Line 339 – just in the denser parts of the agroforest, or throughout their habitat? You did not compare their behavior between microhabitats, so I think this conclusion is unwarranted. Perhaps you could suggest that future studies could compare their behavior in dense vs. open habitat to see if their movement patterns change in areas with better visibility?

Line 343-344 – this sentence is a bit confusing.  How about something like, “Unfortunately, there has been little data on habitats to assist in translocation work.  Habitat data is often absent for an area, vague, or focused on forest connectivity, thereby information on the spatial distribution of key resources required by lorises has not been available to guide translocation efforts”

Line 346- I think this is two separate things.  First, lorises need time to build a cognitive map of their new habitat before they can navigate among resources. Second, there needs to be adequate resources within a habitat distributed in such a way that a loris can establish a home range that gives them access to essential resources.

Line 356- rejects a site and disperses.

Line 356-357- I would cut this sentence as it is repeated below.  

Line 367 – I would rephrase, perhaps something like, “Despite the challenges of translocations, they can be a powerful tool for conserving wild populations if researchers can determine that an area has adequate resources to sustain individuals, and individuals are able to navigate among those resources.”  This is not great, but something like that!

The quality of the language is good.

Author Response

We thank the reviewers for reevaluating this work and all the comments which have helped to improve the article. We addressed all the suggestions and provided clarity where it was needed. Attachment is our responses to each comment.

Author Response File: Author Response.docx